The ribosomal RNA processing machinery is recruited to the nucleolar domain before RNA polymerase I during Xenopus laevis development

Journal of Cell Biology

Volumn 149, Issue 2, 2000, Pages 293-305

  Verheggen, Céline ^a,b   Almouzni, Geneviève ^b   Hernandez Verdun, Danièle ^a  

^a INSTITUT JACQUES MONOD   (France)

^b INSTITUT CURIE   (France)

Author keywords

Nucleologenesis; Pre rRNA; Prenucleolar body; RNA polymerase I transcription; Xenopus laevis development

Indexed keywords

DACTINOMYCIN; DNA DIRECTED RNA POLYMERASE; DNA DIRECTED RNA POLYMERASE III; FIBRILLARIN; MESSENGER RNA; NUCLEOLIN; RIBOSOME RNA; RNA POLYMERASE II; RNA PRECURSOR; SMALL NUCLEAR RIBONUCLEOPROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; FEMALE; GENE FUSION; GENE LOCUS; GENE TARGETING; NONHUMAN; NUCLEOLUS; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; RNA PROCESSING; RNA SPLICING; RNA TRANSCRIPTION; XENOPUS LAEVIS;

ANIMALS; BLASTOCYST; CELL NUCLEOLUS; CHROMOSOMAL PROTEINS, NON-HISTONE; DACTINOMYCIN; EMBRYO, NONMAMMALIAN; FEMALE; GASTRULA; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IN SITU HYBRIDIZATION, FLUORESCENCE; NUCLEAR ENVELOPE; OOCYTES; PHOSPHOPROTEINS; RNA PRECURSORS; RNA, RIBOSOMAL; RNA, SMALL NUCLEAR; RNA-BINDING PROTEINS; TRANSCRIPTION, GENETIC; XENOPUS LAEVIS;

ANIMALIA; XENOPUS LAEVIS;

EID: 0034678358     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.149.2.293     Document Type: Article

References (77)

1. Allmang, C., E. Petfalski, A, Podtelejnikov, M. Mann, D. Tollervey, and P. Mitchell. 1999. The yeast exosome and human PM-Scl are related complexes of 3′-5′ exonucleases. Genes Dev. 13:2148-2158.
2. Almouzni, G. 1998. Assembly of chromatin and nuclear structures in Xenopus egg extract. In Chromatin, A Practical Approach. 195-218.
3. Almouzni, G., and A.P. Wolffe. 1995. Constraints on transcriptional activator function contribute to transcriptional quiescence during early Xenopus embryogenesis. EMBO (Eur. Mol. Biol. Organ.) J. 14:1752-1765.
4. Azum-Gélade, M.-C., J. Noaillac-Depeyre, M. Caizergues-Ferrer, and N. Gas. 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.
5. Bauer, D.W., and J.G. Gall. 1997. Coiled bodies without coilin. Mol. Biol. Cell 8:73-82.
6. Bauer, D.W., C. Murphy, W. Zheng'an, C.H. Wu, and J.G. Gall. 1994. In vitro assembly of coiled bodies in Xenopus egg extract. Mol. Biol. Cell. 5:633-644.
7. Bell, P., and U. Scheer. 1997. Prenucleolar bodies contain coilin and are assembled in Xenopus egg extract depleted of specific nucleolar proteins and U3 RNA. J. Cell Sci. 110:43-54.
8. Bell, P., and U. Scheer. 1999. Developmental changes in RNA polymerase I and TATA box-binding protein during early Xenopus embryogenesis. Exp. Cell Res. 248:122-135.
9. Bell, P., M.C. Dabauvalle, and U. Scheer. 1992. In vitro assembly of prenucleolar bodies in Xenopus egg extract. J. Cell Biol. 118:1297-1304.
10. Bell, P., C. Mais, B. McStay, and U. Scheer. 1997. Association of the nucleolar transcription factor UBF with the transcriptionally inactive rRNA genes of pronuclei and early Xenopus embryos. J. Cell Sci. 110:2053-2063.
11. Benavente, R., K.M. Rose, G. Reimer, B. Hügle-Dörr, and U. Scheer. 1987. Inhibition of nucleolar reformation after microinjection of antibodies to RNA polymerase I into mitotic cells. J. Cell Biol. 105:1483-1491.
12. Bentley, D. 1999. Coupling RNA polymerase II transcription with pre-mRNA processing. Curr. Opin. Cell Biol. 11:347-351.
13. Beven, A.F., R. Lee, M. Razaz, D.J. Leader, J.W.S. Brown, and P.J. Shaw. 1996. The organization of ribosomal RNA processing correlates with the distribution of nucleolar snRNAs. J. Cell Sci. 109:1241-1251.
14. Boudonck, K., L. Dolan, and P.J. Shaw. 1999. The movement of coiled bodies visualized in living plant cells by the green fluorescent protein. Mol. Biol. Cell. 10:2297-2307.
15. Briggs, M.W., K.T.D. Burkard, and J.S. Butler. 1998. Rrp6p, the yeast homologue of the human PM-Scl 100-kDa autoantigen, is essential for efficient 5.8 S rRNA 3′ end formation. J. Biol. Chem. 273:13255-13263.
16. Brown, D.D., and E. Littna. 1964. RNA synthesis during development of Xenopus laevis, the South African clawed toad. J. Mol. Biol. 8:669-687.
17. Corden, J.L., and M. Patturajan. 1997. A CTD function linking transcription to splicing. Trends Biochem. Sci. 22:413-416.
18. Dichtl, B., and D. Tollervey. 1997. Pop3p is essential for the activity of the RNase MRP and RNase P ribonucleoproteins in vivo. EMBO (Eur. Mol. Biol. Organ.) J. 16:417-429.
19. Dundr, M., U.T. Meier, N. Lewis, D. Rekosh, M.-L. Hammarskjöld, and M.O.J. Olson. 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.
20. Duval, C., P. Bouvet, F. Omilli, C. Roghi, C. Dorel, R. LeGuellec, J. Paris, and H.B. Osborne. 1990. Stability of maternal mRNA in Xenopus embryos: role of transcription and translation. Mol. Cell. Biol. 10:4123-4129.
21. Fomproix, N., and Hernandez-Verdun. 1999. Effects of anti-PM-Scl 100 (Rr6p exonuclease) antibodies on prenucleolar body dynamics at the end of mitosis. Exp. Cell Res. 251:452-464.
22. Fomproix, N., J. Gébrane-Younes, and D. Hernandez-Verdun. 1998. Effects of anti-fibrillarin antibodies on building of functional nucleoli at the end of mitosis. J. Cell Sci. 111:359-372.
23. Frey, M.R., A.D. Bailey, A.M. Weiner, and A.G. Matera. 1999. Association of snRNA genes with the coiled bodies is mediated by nascent snRNA transcripts. Curr. Biol. 9:126-135.
24. Gall, J.G., M. Bellini, Z. Wu, and C. Murphy. 1999. Assembly of the nuclear transcription and processing machinery: cajal bodies (coiled bodies) and transcriptosomes. Mol. Biol. Cell. 10:4385-4402.
25. Gautier, T., N. Fomproix, C. Masson, M.C. Azum-Gélade, N. Gas, and D. Hernandez-Verdun. 1994. Fate of specific nucleolar perichromosomal proteins during mitosis: cellular distribution and association with U3 snoRNA. Biol. Cell. 82:81-93.
26. Giménez-Martin, G.C., C. De la Torre, M.E. Fernandez-Gomez, and A. Gonzalez-Fernandez. 1974. Experimental analysis of nucleolar reorganization. J. Cell Biol. 60:502-507.
27. Ginisty, H., F. Amalric, and P. Bouvet. 1998. Nucleolin functions in the first step of ribosomal RNA processing. EMBO (Eur. Mol. Biol. Organ.) J. 17: 1476-1486.
28. Gurdon, J.B., and M.P. Wickens. 1983. Use of Xenopus oocytes for the expression of cloned genes. In Methods in Enzymology. R. Wu, L. Grossman, and K. Moldave, editors. Academic Press, New York. 101:370-386.
29. Hadjiolov, A.A. 1985. The Nucleolus and Ribosome Biogenesis. Vol. 12. M. Alfert, W. Beermann, L. Goldstein, K.R. Porter, and P. Sitte, editors. Springer-Verlag, New York. 268 pp.
30. Highett, M.I., D.J. Rawlins, and P.J. Shaw. 1993. Different patterns of rDNA distribution in Pisum sativum nucleoli correlate with different levels of nucleolar activity. J. Cell Sci. 104:843-852.
31. Huang, S., and D.L. Spector. 1996a. Dynamic organization of pre-mRNA splicing factors. J. Cell Biochem. 62:191-197.
32. Huang, S., and D.L. Spector. 1996b. Intron-dependent recruitment of premRNA splicing factors to sites of transcription. J. Cell Biol. 133:719-732.
33. Jiménez-Garcia, L.F., and D.L. Spector. 1993. In vivo evidence that transcription and splicing are coordinated by a recruiting mechanism. Cell. 73:47-59.
34. Jiménez-Garcia, L.F., L.I. Rothblum, H. Busch, and R.L. Ochs. 1989. Nucleologenesis: use of non-isotopic in situ hybridization and immunocytochemistry to compare the localization of rDNA and nucleolar proteins during mitosis. Biol. Cell. 65:239-246.
35. Jiménez-Garcia, L.F., M.L. Segura-Valdez, R.L. Ochs, L.I. Rothblum, R. Hannan, and D.L. Spector. 1994. Nucleologenesis: U3 snRNA-containing prenucleolar bodies move to sites of active pre-rRNA transcription after mitosis. Mol. Biol. Cell. 5:955-966.
36. Jolly, C., Y. Usson, and R. Morimoto. 1999a. Rapid and reversible relocalization of heat shock factor 1 within seconds to nuclear stress granules. Proc. Natl. Acad. Sci. USA. 96:6769-6774.
37. Jolly, C., C. Vourc'h, M. Robert-Nicoud, and R.I. Morimoto. 1999b. Intron-independent association of splicing factors with active genes. J. Cell Biol. 145:1133-1143.
38. Lamond, A.I., and W.C. Earnshaw. 1998. Structure and function in the nucleus. Science. 280:547-553.
39. Lygerou, Z., C. Allmang, D. Tollervey, and B. Séraphin. 1996a. Accurate processing of a eukaryotic pre-rRNA by RNase MRP in vitro. Science. 272:268-270.
40. Lygerou, Z., H. Pluk, W.J. van Venrooij, and B. Séraphin. 1996b. hPop1: an autoantigenic protein subunit shared by the human RNase P and RNase MRP ribonucleoproteins. EMBO (Eur. Mol. Biol. Organ.) J. 15:5936-5948.
41. Masson, C., C. Bouniol, N. Fomproix, M.S. Szöllösi, P. Debey, and D. Hernandez-Verdun. 1996. Conditions favoring RNA polymerase I transcription in permeabilized cells. Exp. Cell Res. 226:114-125.
42. McCracken, S., N. Fong, K. Yankulov, S. Ballantyne, G. Pan, J. Greenblatt, S.D. Patterson, M. Wickens, and D.L. Bentley. 1997. The C-terminal domain of RNA polymerase II couples mRNA processing to transcription. Nature. 385:357-361.
43. Mebmer, B., and C. Dreyer. 1993. Requirement for nuclear translocation and nucleolar accumulation of nucleolin of Xenopus laevis. Eur. J. Cell. Biol. 61: 369-382.
44. Michot, B., N. Joseph, S. Mazan, and J.P. Bachellerie. 1999. Evolutionarily conserved structural features in the ITS2 of mammalian pre-rRNAs and potential interactions with the snoRNA U8 detected by comparative analysis of new mouse sequences. Nucleic Acids Res. 27:2271-2282.
45. Misteli, T., and D.L. Spector. 1998. The cellular organization of gene expression. Curr. Opin. Cell Biol. 10:323-331.
46. Misteli, T., and D. Spector. 1999. RNA polymerase II targets pre-mRNA splicing factors to transcription sites in vivo. Mol. Cell. 3:697-705.
47. Misteli, T., J.F. Caceres, and D.L. Spector. 1997. The dynamics of a pre-mRNA splicing factor in living cells. Nature. 387:523-527.
48. Mitchell, P., E. Petfalski, A. Shevchenko, M. Mann, and D. Tollervey. 1997. The exosome: a conserved eukaryotic RNA processing complex containing multiple 3′-5′ exoribonucleases. Cell. 91:457-466.
49. Moen, P.T., K.P. Smith, and J.B. Lawrence. 1995. Compartmentalization of specific pre-mRNA metabolism: an emerging view. Hum. Mol. Genet. 4:1779-1789.
50. Morcillo, G., C. De la Torre, and G. Giménez-Martin. 1976. Nucleolar transcription during plant mitosis. Exp. Cell Res. 102:311-316.
51. Newport, J., and M. Kirschner. 1982. A major developmental transition in early Xenopus embryos. I. Characterization and timing of cellular changes at the midblastula stage. Cell. 30:675-686.
52. Nieuwkoop, P.D., and J. Faber. 1994. Normal table of Xenopus laevis (Daudin). Garland Publishing. Inc., New York. 252 pp.
53. Oakes, M., J.P. Aris, J.S. Brockenbrough, H. Wai, L. Vu, and M. Nomura. 1998. Mutational analysis of the structure and localization of the nucleolus in the yeast Saccharomyces cerevisiae. J. Cell Biol. 143:23-34.
54. Ochs, R.L., and K. Smetana. 1991. Detection of fibrillarin in nucleolar remnants and the nucleolar matrix. Exp. Cell Res. 197:183-190.
55. Ochs, R.L., M.A. Lischwe, E. Shen, R.E. Caroll, and H. Busch. 1985a. Nucleologenesis: composition and fate of prenucleolar bodies. Chromosoma. 92:330-336.
56. Ochs, R.L., M.A. Lischwe, W.H. Spohn, and H. Busch. 1985b. Fibrillarin: a new protein of the nucleolus identified by autoimmune sera. Biol. Cell. 54:123-134.
57. Peculis, B.A., and J.A. Steitz. 1993. Disruption of U8 nucleolar snRNA inhibits 5.8S and 28S rRNA processing in the Xenopus oocyte. Cell. 73:1233-1245.
58. Pluk, H., H. Van Eenennaam, S.A. Rutjes, G.J.M. Pruijn, and W.J. Van Venrrooij. 1999. RNA-protein interactions in the human RNase MRP ribonucleoprotein complex. RNA. 5:512-524.
59. Sanford, J.R., and J.P. Bruzik. 1999. Developmental regulation of SR protein phosphorylation and activity. Genes Dev. 13:1513-1518.
60. Savino, T.M., R. Bastos, E. Jansen, and D. Hernandez-Verdun. 1999. The nucleolar antigen Nop 52, the human homologue of the yeast ribosomal RNA processing RRP1, is recruited at late stages of nucleologenesis. J. Cell Sci. 112:1889-1900.
61. Savkur, R.S., and M.O.J. Olson. 1998. Preferential cleavage in pre-ribosomal RNA by protein B23 endoribonuclease. Nucleic Acids Res. 26:4508-4515.
62. Scheer, U., and R. Benavente. 1990. Functional and dynamic aspects of the mammalian nucleolus. Bio Essay. 12:14-20.
63. Scheer, U., M. Thiry, and G. Goessens. 1993. Structure, function and assembly of the nucleolus. Trends Cell Biol. 3:236-241.
64. Scheer, U., and D. Weisenberger. 1994. The nucleolus. Curr. Opin. Cell Biol. 6:354-359.
65. Schmidt-Zachmann, M.S., B. Hügle-Dörr, and W.W. Franke. 1987. A constitutive nucleolar protein identified as a member of the nucleoplasmin family. EMBO (Eur. Mol. Biol. Organ.) J. 6:1881-1890.
66. Shiokawa, K., Y. Misumi, and K. Yamana. 1981a. Demonstration of rRNA synthesis in pre-gastrular embryos of Xenopus laevis. Dev. Growth Differ. 23: 579-587.
67. Shiokawa, K., K. Tashiro, Y. Misumi, and K. Yamana. 1981b. Non-coordinated synthesis of RNA's in pre-gastrular embryos of Xenopus laevis. Dev. Growth Differ. 23:589-597.
68. Smith, C.M., and J.A. Steitz. 1997. Sno storm in the nucleolus: new roles for myriad small RNPs. Cell. 89:669-672.
69. Steinmetz, E.J. 1997. Pre-mRNA processing and the CTD of RNA polymerase II: the tail that wags the dog? Cell. 89:491-494.
70. Thiry, M., and G. Goessens. 1996. The nucleolus during the cell cycle. Springer-Verlag, Heidelberg. 146 pp.
71. Tollervey, D. 1996. Trans-acting factors in ribosome synthesis. Exp. Cell Res. 229:226-232.
72. Trimbur, G.M., and C.J. Walsh. 1993. Nucleolus-like morphology produced during the in vitro reassociation of nucleolar components. J. Cell Biol. 122: 753-766.
73. Van Eenennaam, H., G.J.M. Pruijn, and W.J. Van Venrooij. 1999. hPop4: a new protein subunit of the human RNase MRP and RNase P ribonucleoprotein complexes. Nucleic Acids Res. 27:2465-2472.
74. Verheggen, C., S. Le Panse, G. Almouzni, and D. Hernandez-Verdun. 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. 142:1167-1180.
75. Weisenberger, D., U. Scheer, and R. Benavente. 1993. The DNA topoisomerase I inhibitor camptothecin blocks postmitotic reformation of nucleoli in mammalian cells. Eur. J. Cell Biol. 61:189-192.
76. Xia, L., J. Liu, C. Sage, E.B. Trexler, M.T. Andrews, and E.S. Maxwell. 1995. Intronic U14 snoRNAs of Xenopus laevis are located in two different parent genes and can be processed from their introns during early oogenesis. Nucleic Acids Res. 23:4844-4849.
77. Zatsepina, O.V., O.A. Dudnic, I.T. Todorov, M. Thiry, H. Spring, and M.F. Trendelenburg. 1997. Experimental induction of prenucleolar bodies (PNBs) in interphase cells: interphase PNBs show similar characteristics as those typically observed at telophase of mitosis in untreated cells. Chromosoma. 105:418-430.