Partially processed pre-rRNA is preserved in association with processing components in nucleolus-derived foci during mitosis

Molecular Biology of the Cell

Volumn 9, Issue 9, 1998, Pages 2407-2422

  Dundr, Miroslav ^a   Olson, Mark O J ^a  

^a UNIVERSITY OF MISSISSIPPI MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RIBONUCLEASE; RIBOSOME RNA; RNA PRECURSOR;

ANIMAL CELL; ARTICLE; CELL ORGANELLE; FLUORESCENCE IN SITU HYBRIDIZATION; HELA CELL; HUMAN; HUMAN CELL; MITOSIS; NONHUMAN; NUCLEOLUS; PRIORITY JOURNAL; RNA PROCESSING; RNA SEQUENCE;

ANIMALIA;

EID: 0031670651     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.9.9.2407     Document Type: Article

References (68)

1. Beltrame, M., and Tollervey, D. (1995). Base pairing between U3 and the pre-ribosomal RNA is required for 18S rRNA synthesis. EMBO J. 14, 4350-4356.
2. Beven, A.F., Lee, R., Razaz, M., Leader, D.J., Brown, J.W.S., and Shaw, P.J. (1996). The organization of ribosomal RNA processing correlates with the distribution of nucleolar snRNAs. J. Cell Sci. 109, 1241-1251.
3. Bootsma, D., Budke, L., and Vos, O. (1964). Studies on synchronous division of tissue culture cells initiated by excess thymidine. Exp. Cell Res. 33, 301-309.
4. Chamberlain, J., Pagan-Ramos, E., Kindelberger, D.W., and Engelke, D. (1996). An RNase P RNA subunit mutation affects ribosomal RNA processing. Nucleic Acids Res. 24, 3158-3166.
5. Chu, S., Archer, R.H., Zengel, J.M., and Lindahl, L. (1994). The RNA of RNase MRP is required for normal processing of ribosomal RNA. Proc. Natl. Acad. Sci. USA 91, 659-663.
6. Dunbar, D.A., Wormsley, S., Agentis, T.M., and Baserga, S.J. (1997). Mpp10p, a U3 small nucleolar ribonucleoprotein component required for pre-18S rRNA processing in yeast. Mol. Cell. Biol. 17, 5803-5812.
7. Dundr, M., Leno, G.H., Lewis, N., Rekosh, D., Hammarskjöld, M.-L., and Olson, M.O.J. (1996). Location of the HIV-1 Rev protein during mitosis: inactivation of the nuclear export signal alters the pathway for postmitotic reentry into nucleoli. J. Cell Sci. 109, 2239-2251.
8. Dundr, M., Meier, U.T., Lewis, N., Rekosh, D., Hammarskjöld, M.-L., and Olson, M.O.J. (1997). A class of nonribosomal nucleolar components is located in chromosome periphery and in nucleolus-derived foci during anaphase and telophase. Chromosoma 105, 407-417.
9. Eberhard, D., Tora, L., Egly, J.-M., and Grummt, I. (1993). A TBP-containing multiprotein complex (TIF-IB) mediates transcription specificity of murine RNA polymerase I. Nucleic Acids Res. 21, 4180-4186.
10. Eichler, D.C., and Craig, N. (1994). Processing of eukaryotic ribosomal RNA. Prog. Nucleic Acid Res. Mol. Biol. 49, 197-239.
11. Erickson, J.M., Rushford, C., Dorney, C., Wilson, G., and Schmickel, R. (1981). Structure and variation of human ribosomal DNA: molecular analysis of cloned fragments. Gene 16, 1-9.
12. Erickson, J.M., and Schmickel, R.D. (1985). A molecular basis for discrete size variation in human ribosomal DNA. Am. J. Hum Genet. 37, 311-325.
13. Fan, H., and Penman, S. (1971). Regulation of synthesis and processing of nucleolar components in metaphase-arrested cells. J. Mol. Biol. 59, 27-42.
14. Gautier, T., Dauphin-Villemant, C., André, C., Masson, C., Arnoult, J., and Hernandez-Verdun, D. (1992). Identification and characterization of a new set of nucleolar ribonucleoproteins which line the chromosomes during mitosis. Exp. Cell Res. 200, 5-15.
15. Gébrane-Younès, 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.
16. Gerard, R.D., and Gluzman, Y. (1985). New host cell system for regulated simian virus 40 DNA replication. Mol. Cell. Biol. 5, 3231-3240.
17. Ghisolfi-Nieto, L., Joseph, G., Puvion-Dutilleul, F., Amalric, F., and Bouvet, P. (1996). Nucleolin is a sequence-specific RNA-binding protein: characterization of targets on pre-ribosornal RNA. J. Mol. Biol. 260, 34-53.
18. Ginisty, H., Amalric, F., and Bouvet P. (1998). Nucleolin functions in the first step of ribosomal RNA processing. EMBO J. 17, 1476-1486.
19. Goessens, G. (1984). Nucleolar structure. Int. Rev. Cytol. 87, 107-158.
20. Gottesfeld, J.M., and Forbes, D.J. (1997). Mitotic repression of the transcriptional machinery. Trends Biochem. Sci. 22, 197-202.
21. Gottesfeld, J.M., Wolf, V.J., Dang, T., Forbes, D.J., and Hartl, P. (1994). Mitotic repression of RNA polymerase III transcription in vitro mediated by phosphorylation of a TFIIIB component. Science 263, 81-84.
22. Hadjiolova, K.V., Nicoloso, M., Mazan S., Hadjiolov, A.A., and Bachellerie, J.-P. (1993). Alternative pre-rRNA processing pathways in human cells and their alteration by cycloheximide inhibition of protein synthesis. Eur. J. Biochem. 212, 211-215.
23. Hartl, P., Gottesfeld, J., and Forbes, D.J. (1993). Mitotic repression of transcription in vitro. J. Cell Biol. 120, 613-624.
24. Heix, J., Zomerdijk, J.C., Ravanpav, A., Tjian, R., and Grummt, I. (1997). Cloning of murine RNA polymerase I-specific TAFs: conserved interactions between the four subunits of the species-specific transcription factor TIF-IB/SL1. Proc. Natl. Acad. Sci. USA 94, 1733-1738.
25. Heliot, L., Kaplan, H., Lucas, L., Klein, C., Beorchia, A., Doco-Fenzy, M., Menager, M., Thiry, M., O'Donohue, M.-F., and Ploton, D. (1997). Electron tomography of metaphase nucleolar organizer regions: evidence for a twisted-loop organization. Mol. Biol. Cell. 8, 2199-2216.
26. Hernandez-Verdun, D., and Gautier, T. (1994). The chromosome periphery during mitosis. Bioessays 16, 179-185.
27. Hughes, J.M.X., and Ares, M. (1991). Depletion of U3 small nucleolar RNA inhibits cleavage in the 5′ external transcribed spacer of yeast pre-ribosomal RNA and impairs formation of 18S ribosomal RNA. EMBO J. 10, 4231-4239.
28. Jacobson, M.R., Cao, L.-G., Taneja, K., Singer, R.H., Wang, Y., and Pederson, T. (1997). Nuclear domains of the RNA subunit of RNase P. J. Cell Sci. 110, 829-837.
29. Jiménez-García, 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.
30. Jordan, P., Mannervik, M., Tora, L., and Carmo-Fonseca, M. (1996). 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, 225-234.
31. Kass, S., Tyc, K., Steitz, J.A., Sollner-Webb, B. (1990). The U3 small nucleolar ribonucleoprotein functions in the first step of preribosomal processing. Cell 60, 897-908.
32. Lazdins, I.B., Delannoy, M., and Sollner-Webb, B. (1997). Analysis of nucleolar transcription and processing domains and pre-rRNA movements by in situ hybridization. Chromosoma 105, 481-495.
33. Leresche, A., Wolf, V.J., and Gottesfeld, J.M. (1996). Repression of RNA polymerase II and III transcription during M phase of the cell cycle. Exp. Cell Res. 229, 282-288.
34. Li, H.D., Zagorski, J.J., and Fournier, M.J. (1990). Depletion of U14 small nuclear RNA (snR128) disrupts production of 18S rRNA in Saccharomyces cerevisiae. Mol. Cell. Biol. 10, 1145-1152.
35. Liang, W.-Q., and Fournier, M.J. (1995). U14 base-pairs with 18S rRNA: a novel snoRNA interaction required for rRNA processing. Genes Dev. 9, 2433-2443.
36. Lygerou, Z., Allmang, C., Tollervey, D., and Séraphin, B. (1996a). Accurate processing of a eukaryotic pre-rRNA by RNase MRP in vitro. Science 272, 268-270.
37. Lygerou, Z., Mitchell, P., Petfalski, E., Séraphin, B., and Tollervey, D. (1994). The POP1 gene encodes a protein component common to the RNase MRP and RNase P ribonucleoproteins. Genes Dev. 8, 1423-1433.
38. Lygerou, Z., Pluk, H., van Venrooij, W.J., and Séraphin, B. (1996b). hPop1: an autoantigenic protein subunit shared by the human RNase P and RNase MRP ribonucleoproteins. EMBO J. 15, 5936-5948.
39. Maden, B.E.H., and Hughes, J.M.X. (1997). Eukaryotic ribosomal RNA: the recent excitement in the nucleotide modification problem. Chromosoma 105, 391-400.
40. Matera, A.C., Tycowski, K.T., Steitz, J.A., and Ward, D.C. (1994). Organization of small nucleolar ribonucleoproteins (snoRNPs) by fluorescence in situ hybridization and immunocytochemistry. Mol. Biol. Cell 5, 1289-1299.
41. Maxwell, E.S., and Fournier, M.J. (1995). The small nucleolar RNAs. Annu. Rev. Biochem. 35, 897-934.
42. Medina, F.J., Cerdido, A., and Fernández-Gómez, M.E. (1995). Components of the nucleolar processing complex (pre-rRNA, Fibrillarin, and Nucleolin) colocalize during mitosis and are incorporated to daughter cell nucleoli. Exp. Cell Res. 221, 111-125.
43. Mougey, E.B., O'Reilly, M., Osheim, Y., Miller, O.L., Jr., Beyer, A., and Sollner-Webb, B. (1993a). The terminal balls characteristic of eukaryotic rRNA transcription units in chromatin spreads are rRNA processing complexes. Genes Dev. 7, 1609-1619.
44. Mougey, E.B., Pape, L.K., and Sollner-Webb, B. (1993b). A U3 small nuclear ribonucleoprotein-requiring processing in the 5′ external transcribed spacer of Xenopus precursor rRNA. Mol. Cell. Biol. 13, 5990-5998.
45. Peculis, B.A., and Steitz, J.A. (1993). Disruption of U8 nucleolar snRNA inhibits 5.8S and 28S rRNA processing in the Xenopus oocyte. Cell 73, 1233-1245.
46. Phillips, D.M., and Phillips, S.G. (1973). Repopulation of postmitotic nucleoli by preformed RNA. J. Cell Biol. 58, 54-663.
47. Prescott, D.M., and Bender, M.A. (1962). Synthesis of RNA and protein during mitosis in mammalian tissue culture cells. Exp. Cell Res. 26, 260-268.
48. Puvion-Dutilleul, F., Puvion, E., and Bachellerie, J.-P. (1997). Early stages of pre-rRNA formation within the nucleolar ultrastructure of mouse cells studied by in situ hybridization with a 5′ETS leader probe. Chromosoma 105, 496-505.
49. 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.
50. Savino, R., and Gerbi, S.A. (1990). In vivo disruption of Xenopuf U3 snRNA affects ribosomal RNA processing. EMBO J. 9, 2299-2308.
51. Scheer, U., and Benavente, R. (1990). Functional and dynamic aspects of the mammalian nucleolus. Bioessays 12, 14-21.
52. Scheer, U., Thiry, M., and Goessens, G. (1993). Structure, function and assembly of the nucleolus. Trends Cell Biol. 3, 236-241.
53. Schmitt, M.E., and Clayton, D.A. (1992). Yeast site-specific ribonucleoprotein endoribonuclease MRP contains an RNA component homologous to mammalian RNase MRP and essential for cell viability. Genes Dev. 6, 1975-1985.
54. Schnapp, A., and Grummt, I. (1991). Transcription complex formation at the mouse rDNA promoter involves the stepwise association of four transcription factors and RNA polymerase I. J. Biol. Chem. 266, 24588-24595.
55. Segil, N., Guermah, M., Hoffmann, A., Roeder, R.G., and Heintz, N. (1996). Mitotic regulation of TFIID: inhibition of activator-dependent transcription and changes in subcellular localization. Genes Dev. 10, 2389-2400.
56. Seither, P., Zatsepina, O., Hoffmann, M., and Grummt, I. (1997). Constitutive and strong association of PAF53 with RNA polymerase I. Chromosoma 106, 216-225.
57. Shaw, P.J., and Jordan, E.G. (1995). The nucleolus. Annu. Rev. Cell Dev. Biol. 11, 93-121.
58. Sollner-Webb, B., Tyc, K., and Steitz, J.A. (1996). Ribosomal RNA processing in eukaryotes. In: Ribosomal RNA: Structure, Evolution, Processing and Function in Protein Synthesis, ed. R. Zimmerman and A. Dahlberg, Boca Raton, FL: CRC Press, 469-490.
59. Stole, V., and Altman, S. (1997). Rpp1, an essential protein subunit of nuclear RNase P required for processing of precursor tRNA and 35S precursor rRNA in Saccharomyces cerevisiae. Genes Dev. 11, 2926-2937.
60. Suja, J.A., Gébrane-Younès, J., Géraud, G., and Hernandez-Verdun, D. (1997). Relative distribution of rDNA and proteins of the RNA polymerase I transcription machinery at chromosomal NORs. Chromosoma 105, 459-469.
61. Tollervey, D., and Kiss, T. (1997). Function and synthesis of small nucleolar RNAs. Curr. Opin. Cell Biol. 9, 337-342.
62. Tuteja, N., et al. (1995). Human DNA helicase IV is nucleolin, an RNA helicase modulated by phosphorylation. Gene 160, 143-148.
63. Voit, R., Schäfer, K., and Grummt, I. (1997). Mechanism of repression of RNA polymerase I transcription by the retinoblastoma protein. Mol. Cell. Biol. 17, 4230-4237.
64. 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.
65. Westendorf, J.M., Konstantinov, K.N., Wormsley, S., Shu, M.D., Matsumoto-Taniura, N., Pirollet, F., Klier, F.G., Gerace, L., and Baserga, S.J. (1998). M phase phosphoprotein 10 is a human U3 small nucleolar ribonucleoprotein component. Mol. Biol. Cell 9, 437-449.
66. White, R.J., Gottlieb, T.M., Dowries, C.S., and Jackson, S.P. (1995). Cell cycle regulation of RNA polymerase III transcription. Mol. Cell. Biol. 15, 6653-6662.
67. Wilson, G.N., Szura, L.L., Rushford, C., Jackson, D., and Erickson, J. (1982). Structure and variation of human ribosomal DNA: the external transcribed spacer and adjacent regions. Am. J. Hum. Genet. 34, 32-49.
68. Zatsepina, O.V., Dudnic, O.A., Chentsov, Y.S., Thiry, M., Spring, H., and Tredelenburg, M.F. (1997). Reassembly of functional nucleoli following in situ unraveling by low-ionic-strength of cultured mammalian cells. Exp. Cell Res. 233, 155-168.