Nucleolin functions in the first step of ribosomal RNA processing

EMBO Journal

Volumn 17, Issue 5, 1998, Pages 1476-1486

  Ginisty, Hervé ^a   Amalric, François ^a   Bouvet, Philippe ^a  

^a CNRS   (France)

Author keywords

Nucleolin; Ribosome biogenesis; rRNA processing; Small nucleolar RNA

Indexed keywords

NUCLEOLIN; RIBOSOME RNA; RNA PRECURSOR; SMALL NUCLEAR RIBONUCLEOPROTEIN;

ANIMAL CELL; ARTICLE; GENETIC CONSERVATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; RNA PROCESSING;

ANIMALS; BASE SEQUENCE; CONSERVED SEQUENCE; CROSS-LINKING REAGENTS; MICE; PHOSPHOPROTEINS; PROTEIN BINDING; RECOMBINANT PROTEINS; RNA PRECURSORS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, RIBOSOMAL; RNA, SMALL NUCLEAR; RNA-BINDING PROTEINS; ULTRAVIOLET RAYS;

ANIMALIA; METAZOA;

EID: 0032473356     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.5.1476     Document Type: Article

References (66)

1. Abou Elela,S., Igel,H. and Ares,M. (1996) RNase III cleaves eukaryotic pre-ribosomal RNA at a U3 snoRNP-dependent site. Cell, 85, 115-124.
2. Bach,R., Grummt,I. and Allet,B. (1981) The nucleotide sequences of the initiation region of the ribosomal transcription unit from mouse. Nucleic Acids Res., 9, 1559-1569.
3. Belenguer,P., Baldin,V., Mathieu,C., Prats,H., Bensaid,M., Bouche,G. and Amalric,F. (1989) Protein kinase NII and the regulation of rDNA transcription in mammalian cells. Nucleic Acids Res., 17, 6625-6636.
4. Belenguer,P., Caizergues-Ferrer,M., Labbé,J.C., Dorée,M. and Amalric,F. (1990) Mitosis-specific phosphorylation of nucleolin by p34cdc2 protein kinase. Mol. Cell. Biol, 10, 3607-3618.
5. Beltrame,M. and Tollervey,D. (1992) Identification and functional analysis of two U3 binding sites on yeast pre-ribosomal RNA. EMBO J., 11, 1531-1542.
6. Bharti,AK., Olson,M.OJ., Kufe,D.W. and Rubin,E.H. (1996) Identification of a nucleolin binding site in human topoisomerase I. J. Biol. Chem., 271, 1993-1997.
7. Blum,B., Pierron,G., Seebeck,T. and Braun,R. (1986) Processing in the external transcribed spacer of ribosomal RNA from Physarum polycephalum. Nucleic Acids Res., 14, 3153-3166.
8. Bouche,G., Caizergues-Ferrer,M., Bugler,B. and Amalric,F. (1984) Interrelations between the maturation of a 100 KDa nucleolar protein and pre-rRNA synthesis in CHO cells. Nucleic Acids Res., 12, 3025-3035.
9. Bouche,G., Baldin,V., Belenguer,P., Prats,H. and Amalric,F. (1994) Activation of rDNA transcription by FGF-2: key role of protein kinase CKII. Cell. Mol. Biol. Res., 40, 547-554.
10. Bourbon,H., Bugler,B., Caizergues-Ferrer,M. and Amalric,F. (1983a) Role of phosphorylation on the maturation pathways of a 100 KDa nucleolar protein. FEBS Lett., 155, 218-222.
11. Bourbon,H.M., Bugler,B., Caizergues-Ferrer,M., Amalric,F. and Zalta,J.P. (1983b) Maturation of a 100kDa protein associated with preribosomes in Chinese hamster ovary cells. Mol. Biol. Rep., 9, 39-47.
12. Bourquin,J.P., Stagljar.I., Meier,P., Moosmann,P., Silke,J., Baechi,T., Georgiev,O. and Schaffner,W. (1997) A serine/arginine-rich nuclear matrix cyclophilin interacts with the C-terminal domain of RNA polymerase II. Nucleic Acids Res., 25, 2055-2061.
13. Bouvet,P. Jain,C., Belasco,J., Amalric,F. and Erard,M. (1997) RNA recognition by the joint action of two nucleolin RNA-binding domains: genetic analysis and structural modeling. EMBO J., 16, 5235-5246.
14. Bugler,B., Caizergues-Ferrer,M., Bouche,G. Bourbon,H. and Amalric.F. (1982) Detection and localization of a class of proteins immunologically related to a 100-KDa nucleolar protein. Eur. J. Biochem., 328, 473-480.
15. Bugler,B., Bourbon,H., Lapeyre,B., Wallace,M.O., Chang,J.H., Amalric,F. and Olson,M.O.J. (1987) RNA binding fragments from nucleolin contain the ribonucleoprotein consensus sequence. J. Biol. Chem., 262, 10922-10925.
16. Caizergues-Ferrer,M., Belenguer,P., Lapeyre,B., Amalric,F., Wallace,M.O. and Olson,M.O.J. (1987) Phosphorylation of nucleolin by a nucleolar type NII protein kinase. Biochemistry, 26, 7876-7883.
17. Craig,N., Kass,S. and Sollner-Webb,B. (1987) Nucleotide sequence determining the first cleavage site in the processing of mouse precursor rRNA. Proc. Natl Acad. Sci. USA, 84, 629-633.
18. Craig,N., Kass,S. and Sollner-Webb,B. (1991) Sequence organization and RNA structural motifs directing the mouse primary rRNA-processing event. Mol. Cell. Biol., 11, 458-467.
19. Egyhazi,E., Pigon,A., Chang,J.H., Ghaffari,S.H., Dressen,T.D., Wellman,S.E., Case,S.T.S. and Olson,M.O.J. (1988) Effect of anti C23 (nucleolin) antibody on transcription of ribosomal DNA in Chironomus salivary gland cells. Exp. Cell Res., 178, 264-272.
20. Eichler,D.C. and Craig,N. (1994) Processing of eukaryotic ribosomal RNA. Prog. Nucleic Acid Res. Mol. Biol., 49, 197-237.
21. Eichler,D.C. and Eales,S.J. (1982) Isolation and characterization of a single-stranded specific endoribonuclease from Ehrlich cell nucleoli. J. Biol. Chem., 257, 14384-14389.
22. Enright,C.A., Maxwell,E.S. and Sollner-Webb,B. (1996) 5′ETS rRNA processing facilitated by four small RNAs: U14, E3, U17 and U3. RNA, 2, 1094-1099.
23. Erard,M., Belenguer,P., Caizergues-Ferrer,M. Pantaloni,A. and Amalric,F. (1988) A major nucleolar protein, nucleolin, induces chromatin decondensation by binding to histone H1. Eur. J. Biochem., 175, 525-530.
24. Escande,M.L., Azum,M.C., Tichadou,J.L. and Gas,N. (1985) Correlation between rDNA transcription and distribution of a 100 kDa nucleolar protein in CHO cells. Exp. Cell Res., 161, 353-363.
25. Ghisolfi,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-ribosomal RNA. J. Mol. Biol, 260, 34-53.
26. Gurney,T.J. (1985) Characterization of mouse 45S ribosomal RNA subspecies suggests that the first processing cleavage occurs 600 ± 100 nucleotides from the 5′ end and the second 500 ± 100 nucleotides from the 3′ end of a 13.9 kb precursor. Nucleic Acids Res., 13, 4905-4919.
27. Hadjiolov,A.A. (1985) The nucleolus and ribosome biogenesis. Alfert,M., Beermann,W., Goldstein,L., Porter,K.R. and Sitte,P. (eds), Cell Biology Monographs. Springer-Verlag, Berlin.
28. Hanakahi,L.A., Dempsey,L.A., Li,M.J. and Maizels,N. (1997) Nucleolin is one of the B cell-specific transcription factor and switch region binding protein, LR1. Proc. Natl Acad. Sci. USA, 94, 3605-3610.
29. Herrera,A.H. and Olson,M.O.J. (1986) Association of protein C23 with rapidly labeled nucleolar RNA. Biochemistry, 25, 6258-6264.
30. Hugues,J.M.X. and Ares,M.,Jr (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, 4239-4239.
31. Kass,S. and Sollner-Webb,B. (1990) The first pre-rRNA processing event occurs in a large complex: analysis by gel retardation, sedimentation, and UV crosslinking. Mol. Cell. Biol., 10, 4920-4931.
32. Kass,S., Craig,N. and Sollner-Webb,B. (1987) Primary processing of mammalian rRNA involves two adjacent cleavages and is not species specific. Mol. Cell. Biol. 7, 2891-2898.
33. Kass,S., Tyc,K., Steitz,J.A. and Sollner-Webb,B. (1990) The U3 small nucleolar ribonucleoprotein functions in the first step of preribosomal RNA processing. Cell, 60, 897-908.
34. Kharrat,A., Derancourt,J., Dorée,M., Amalric,F. and Erard,M. (1991) Synergistic effect of histone H1 and nucleolin on chromatin condensation in mitosis: role of a phosphorylated heteromer. Biochemistry, 30, 10329-10336.
35. Kim,E., Du,L., Bregman,D.B. and Warren,S.L. (1997) Splicing factors associate with hyperphosphorylated RNA polymerase II in the absence of pre-mRNA. J. Cell Biol., 136, 19-28.
36. Lübben,B., Marshallsay,C., Rottmann,N. and Lührmann,R. (1993) Isolation of U3 snoRNP from CHO cells: a novel 55 kDa protein binds to the central part of U3 snoRNA. Nucleic Acids Res., 21, 5377-5385.
37. Maden,B.E.H. (1990) The numerous modified nucleotides in eukaryotic ribosomal RNA. Prog. Nucleic Acids Res. Mol. Biol., 39, 241-301.
38. Maser,R.L. and Calvet,J.P. (1989) U3 small nuclear RNA can be psoralencross-linked in vivo to the 5′ external transcribed spacer of preribosomal-RNA. Proc. Natl Acad. Sci. USA, 86, 6523-6527.
39. Maxwell,E.S. and Fournier,M.J. (1995) The small nucleolar RNAs. Annu. Rev. Biochem., 35, 897-934.
40. McCracken,S., Fong,N., Yankulov,K., Ballantyne,S., Pan.G., Greenblatt,J., Patterson,S., Wickens,M. and Bentley,D.L. (1997) The C-terminal domain of RNA polymerase II couples mRNA processing to transcription. Nature, 385, 357-361.
41. Michot,B. and Bachellerie,J.P. (1991) Secondary structure of the 5′ external transcribed spacer of vertebrate pre-rRNA: presence of phylogenetically conserved features. Eur. J. Biochem., 195, 601-609.
42. Miesfeld,R. and Arnheim,N. (1982) Identification of the in vivo and in vitro origin of transcription in human rDNA. Nucleic Acids Res., 10, 3933-3949.
43. Miller,K.G. and Sollner-Webb,B. (1981) Transcription of mouse rRNA gene by RNA polymerase I: in vivo and in vitro initiation and processing sites. Cell, 27, 165-174.
44. Miller,O.L.,Jr and Bakken,A-H. (1972) Morphological studies of transcription. In Diczfaly,E. (ed.), Gene Transcription in Reproductive Tissue. Karolina Instituted Stockholm, pp. 155-177.
45. Miller,O.L.,Jr and Beatty,B.R. (1969) Visualization of nucleolar genes. Science, 164, 955-957.
46. Mougey,E.B., Pape,L.K. and Sollner-Webb,B. (1993a) A U3 small nuclear ribonucleoprotein-requiring processing event in the 5′ external transcribed spacer of Xenopus precursor rRNA. Mol. Cell. Biol., 13, 5990-5998.
47. Mougey,E.B., O'Reilly,M., Osheim,Y., Miller,O.L., Beyer,A. and Sollner-Webb,B. (1993b) The terminal balls characteristic of eukaryotic rRNA transcription units in chromatin spreads are rRNA processing complexes. Genes Dev., 7, 1609-1619.
48. Ohmori,H. et al. (1990) Simultaneous activation of heat shock protein (hsp 70) and nucleolin genes during in vivo and in vitro prereplicative stages of rat hepatocytes. Exp. Cell Res., 189, 227-232.
49. Olson,M.O.J., Rivers,Z.M., Thompson,B.A., Kao,W.-Y. and Case,S.T. (1983) Interaction of nucleolar phosphoprotein C23 with cloned segments of rat ribosomal deoxyribonucleic acid. Biochemistry, 22, 3345-3351.
50. Parker,K.A. and Steitz,J.A. (1987) Structural analyses of the human U3 ribonucleoprotein particle reveal a conserved sequence available for base pairing with pre-rRNA. Mol. Cell. Biol., 7, 2899-2913.
51. Peter,M., Nakagawa,J., Dorée,M., Labbé,J.C. and Nigg,E.A. (1990) Identification of major nucleolar proteins as candidate mitotic substrates of cdc2 kinase. Cell, 60, 791-801.
52. Puvion-Dutilleul,F., Bachellerie,J.-P, Zalta,J.-P. and Bernhard,W. (1977) Morphology of ribosomal transcription units in isolated subnuclear fractions of mammalian cells. Biol. Cell., 30, 183-194.
53. Savino,R. and Gerbi,S.A. (1991) Preribosomal RNA processing in Xenopus oocytes does not include cleavage within the external transcribed spacer as an early step. Biochimie, 73, 805-812.
54. Serin,G., Joseph,G., Faucher,C., Ghisolfi,L., Bouche,G., Amalric,F. and Bouvet,P. (1996) Localization of nucleolin binding sites on human and mouse pre-ribosomal RNA. Biochimie, 78, 530-538.
55. Serin,G., Joseph,G., Ghisolfi,L., Bauzan,M., Erard,M., Amalric,F. and Bouvet,P. (1997) Two RNA-binding domains determine the RNA-binding specificity of nucleolin. J. Biol. Chem., 272, 13109-13116.
56. Scheer,U. and Benavente,R. (1990) Functional and dynamic aspects of the mammalian nucleolus. BioEssays, 12, 14-20.
57. Shumard,C.M. and Eichler,D.C. (1988) Ribosomal RNA processing: limited cleavages of mouse preribosomal RNA by a nucleolar endoribonuclease include the early +650 processing site. J. Biol. Chem., 263, 19346-19352.
58. Sirri,V., Roussel,P., Trerè,D., Derenzini,M. and Hernandez-Verdun,D. (1995) Amount variability of total and individual Ag-NOR proteins in cells stimulated to proliferate. J. Histochem. Cytochem., 43, 887-893.
59. Stroke,I.L. and Weiner,A.M. (1989) The 5′ end of U3 snRNA can be crosslinked in vivo to the external transcribed spacer of rat ribosomal RNA precursors. J. Mol. Biol., 210, 497-512.
60. Suzuki,N., Matsui,H. and Hosoya,T. (1985) Effects of androgen and polyamines on the phosphorylation of nucleolar proteins from rat ventral prostates with particular reference to 110-kDa phosphoprotein. J. Biol Chem., 260, 8050-8055.
61. Tollervey,D. (1996) Trans-acting factors in ribosome synthesis. Exp. Cell Res., 229, 226-232.
62. Tyc,K. and Steitz,J.A. (1992) A new interaction between the mouse 5′ external transcribed spacer of pre-rRNA and U3 snRNA detected by psoralen crosslinking. Nucleic Acids Res., 20, 5375-5382.
63. Urano,Y., Kominami,R., Mishima,Y. and Muramatsu,M. (1980) The nucleotide sequence of the putative transcription initiation site of a cloned ribosomal RNA gene of the mouse. Nucleic Acids Res., 8, 6043-6058.
64. Warrener,P. and Petryshyn,R. (1991) Phosphorylation and proteolytic degradation of nucleolin from 3T3-F442A cells, Biochem. Biophys. Res. Commun., 180, 716-723.
65. Yang,T.-H., Tsai,W.-H., Lee,Y.-M., Lei,H.-Y., Lai,M.-Y, Chen,D.-S., Yeh,N.-S and Lee,S.-C. (1994) Purification and characterization of nucleolin and its identification as a transcription represser. Mol. Cell. Biol, 14, 6068-6074.
66. Yuryev,A., Patturajan,M., Litingtung,Y., Joshi,R.V., Gentile,C., Gebara,M. and Corden,J.L. (1996) The C-terminal domain of the largest subunit of RNA polymerase II interacts with a novel set of serine/arginine-rich proteins. Proc. Natl Acad. Sci. USA, 93, 6975-6980.