Nucleolin is a sequence-specific RNA-binding protein: Characterization of targets on pre-ribosomal RNA

Journal of Molecular Biology

Volumn 260, Issue 1, 1996, Pages 34-53

  Ghisolfi Nieto, Laurence ^a   Joseph, Gérard ^a   Puvion Dutilleul, Francine ^b   Amalric, François ^a   Bouvet, Philippe ^a  

^a Institut de Biochimie et Genetique Cellulaires   (France)

^b Integration des Fonctions C   (France)

Author keywords

Nucleolin; Ribosome biogenesis; RNA structure; RNA binding protein; SELEX

Indexed keywords

NUCLEOLIN; RNA BINDING PROTEIN; SMALL NUCLEAR RIBONUCLEOPROTEIN;

ANIMAL CELL; ARTICLE; BIOGENESIS; DISSOCIATION CONSTANT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN RNA BINDING; PROTEIN TARGETING; RIBOSOME; RNA SEQUENCE; RNA STRUCTURE; SEQUENCE HOMOLOGY;

EID: 0030570466     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1996.0380     Document Type: Article

References (64)

1. Adam, S. A., Nakagawa, T., Swanson, M. S., Woodruff, T. K. & Dreyfuss, G. (1986). mRNA polyadenylate-binding protein: gene isolation and sequencing and identification of a ribonucleoprotein consensus sequence. Mol. Cell. Biol. 6, 2932-2943.
2. Bachellerie, J. P., Michot, B., Nicoloso, M., Balakin, A., Ni, J. & Fournier, M. J. (1995). Antisense snoRNAs: a family of nucleolar RNAs with long complementarities to rRNA. Trends Biochem. Sci. 20, 261-264.
3. Belenguer, P., Baldin, V., Mathieu, C., Prats, H., Bensaid, M., Bouche, G. & Amalric, F. (1989). Protein kinase NII and the regulation of rDNA transcription in mammalian cells. Nucl. Acids Res. 17, 6625-6636.
4. Beltrame, M., Henry, Y. & Tollervey, D. (1994). Mutational analysis of an essential binding site of this U3 snoRNA in the 5′ external transcribed spacer of pre-rRNA. Nucl. Acids Res. 23, 5139-5147.
5. Bentley, R. C. & Keene, J. D. (1991). Recognition of U1 and U2 small nuclear RNAs can be altered by a 5-amino-acid segment in the U2 small nuclear ribonucleoprotein particle (snRNP) B" protein and through interactions with U2 snRNP-A' protein. Mol. Cell. Biol. 11, 1829-1839.
6. Birney, E., Kumar, S. & Krainer, A. R. (1993). Analysis of the RNA recognition motif and RS and RGG domains: conservation in metazoan pre-mRNA splicing factors. Nucl. Acids Res. 21, 5803-5816.
7. Borer, R. A., Lehner, C. F., Eppenberger, H. M. & Nigg, E. A. (1989). Major nucleolar proteins shuttle between nucleus and cytoplasm. Cell, 56, 379-390.
8. Bouche, G., Caizergues-Ferrer, M., Bugler, B. & Amalric, F. (1984). Interrelations between the maturation of a 100 kDa nucleolar protein and pre-rRNA synthesis in CHO cells. Nucl. Acids Res. 12, 3025-3035.
9. Bourbon, H., Bugler, B., Caizergues-Ferrer, M. & Amalric, F. (1983). Role of phosphorylation on the maturation pathways of a 100 kDa nucleolar protein. FEBS Letters, 155, 218-222.
10. Bourbon, H., Michot, B., Hassouna, N., Feliu, J. & Bachellerie, J.-P. (1988). Sequence and secondary structure of the 5′ external transcribed spacer of mouse pre-rRNA. DNA, 7, 181-191.
11. Bugler, B., Caizergues-Ferrer, M., Bouche, G., Bourbon, H. & Amalric, F. (1982). Detection and localization of a class of proteins immunologically related to a 100-KDa nucleolar protein. Eur. J. Biochem. 128, 475-480.
12. Bugler, B., Bourbon, H., Lapeyre, B., Walace, M. O., Chang, J. H., Amalric, F. & Olson, M. O. J. (1987). RNA binding fragments from nucleolin contain the ribonucleoprotein consensus sequence. J. Biol. Chem. 262, 10922-10925.
13. Burd, C. G. & Dreyfuss, G. (1994a). Conserved structures and diversity of functions of RNA-binding proteins. Science, 265, 615-621.
14. Burd, C. G. & Dreyfuss, G. (1994b). RNA-binding specificity of hnRNP A1: significance of hnRNP A1 high-affinity binding sites in pre-mRNA splicing. EMBO J. 13, 1197-1204.
15. Burd, C. G., Matunis, E. & Dreyfuss, G. (1991). The multiple RNA-binding domains of the mRNA poly(A)-binding protein have different RNA-binding activities. Mol. Cell. Biol. 11, 3419-3424.
16. Caizergues-Ferrer, M., Belenguer, P., Lapeyre, B., Amalric, F., Wallace, M. O. & Olson, M. O. J. (1987). Phosphorylation of nucleolin by a nucleolar type NII protein kinase. Biochemistry, 26, 7876-7883.
17. Carey, J. & Uhlenbeck, O. C. (1983). Kinetic and thermodynamic characterisation of the R17 coat protein-ribonucleic acid interaction. Biochemistry, 22, 2610-2625.
18. Chauveau, J., Moule, Y. & Rouiller, C. (1956). Isolation of pure and unaltered liver nuclei. Morphology and biochemical composition. Exp. Cell Res. 11, 317-331.
19. Egyhazi, E., Pigon, A., Chang, J. H., Ghaffari, S. H., Dressen, T. D., Wellman, S. E., Case, S. T. S. & 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. & Craig, N. (1994). Processing of eukaryotic ribosomal RNA. Prog. Nucl. Acid Res. Mol. Biol. 49, 197-237.
21. Escande, M. L., Gas, N. & Stevens, B. J. (1985). Immunolocalisation of the 100 K nucleolar protein in CHO cells. Biol. Cell. 53, 99-109.
22. Garret, D. S., Lodi, P. J., Shamoo, Y., Williams, K. R., Clore, G. M. & Gronenborn, A. M. (1994). Determination of the secondary structure and folding topology of an RNA binding domain of mammalian hnRNP A1 protein using three-dimensional heteronuclear magnetic resonance spectroscopy. Biochemistry, 33, 2852-2858.
23. Ghisolfi, L., Joseph, G., Amalric, F. & Erard, M. (1992a). The glycine-rich domain of nucleolin has an unusual supersecondary structure responsible for its RNA-helix-destabilizing properties. J. Biol. Chem. 267, 2955-2959.
24. Ghisolfi, L., Kharrat, A., Joseph, G., Amalric, F. & Erard, M. (1992b). Concerted activities of the RNA recognition and the glycine-rich C-terminal domains of nucleolin are required for efficient complex formation with pre-ribosomal RNA. Eur. J. Biochem. 209, 541-548.
25. Görlach, M., Wittekind, M., Beckman, R. A., Mueller, L. & Dreyfuss, G. (1992). Interaction of the RNA-binding domain of the hnRNP C proteins with RNA. EMBO J. 11, 3289-3295.
26. Görlach, M., Burd, C. G. & Dreyfuss, G. (1994a). The determinants of RNA-binding specificity of the heterogenous nuclear ribonucleoprotein C proteins. J. Biol. Chem. 269, 23074-23078.
27. Görlach, M., Burd, C. G. & Dreyfuss, G. (1994b). The mRNA poly(A) binding protein: localization, abundance, and RNA-binding specificity. Exp. Cell Res. 211, 400-407.
28. Grummt, I., Sollner-Webb, C. & Scholz, I. (1979). Characterisation of a cloned ribosomal fragment from mouse which contains the 18 S coding region and adjacent spacer sequences. Nucl. Acids Res. 6, 1351-1369.
29. Herrera, A. H. & Olson, M. O. J. (1986). Association of protein C23 with rapidly labeled nucleolar RNA. Biochemistry, 25, 6258-6264.
30. Hoffman, D. W., Query, C. C., Golden, B. L., White, S. W. & Keene, J. D. (1991). RNA-binding domain of the A protein component of the U1 small nuclear ribonucleoprotein analyzed by NMR spectroscopy is structurally similar to ribosomal proteins. Proc. Natl Acad. Sci. USA, 88, 2495-2499.
31. Howe, P. W., Nagai, K., Neuhaus, D. & Varani, G. (1994). NMR studies of U1 snRNA recognition by the N-terminal RNP domain of the human U1A protein. EMBO J. 13, 3873-3881.
32. Kass, S. & Sollner-Webb, B. (1990). The first pre-rRNA processing event occurs in a large complex: analysis by gel retardation, sedimentation, and UV cross-linking. Mol. Cell. Biol. 10, 4920-4931.
33. Kass, S., Tyc, K., Steitz, J. A. & Sollner-Webb, B. (1990). The U3 small nucleolar ribonucleoprotein functions in the first step of preribosomal RNA processing. Cell, 60, 897-908.
34. Kühn, U. & Pieler, T. (1996). Xenopus poly(A) binding protein: functional domains in RNA binding and protein-protein interaction. J. Mol. Biol. 256, 20-30.
35. Lee, A. L., Kanaar, R., Rio, D. C. & Wemmer, D. E. (1994). Resonance assignments and solution structure of the second RNA-binding domain of sex-lethal determined by multidimensional heteronuclear magnetic resonance. Biochemistry, 33, 13775-13786.
36. Lee, P. L., Johnson, D. E., Cousens, L. S., Fried, V. A. & Williams, L. T. (1989). Purification and complementary DNA cloning of a receptor for Basic Fibroblast Growth Factor. Science, 245, 57-60.
37. Lutz-Freyermuth, C., Query, C. C. & Keene, J. D. (1990). Quantitative determination that one of two potential RNA-binding domains of a A protein component of the U1 small nuclear ribonucleoprotein complex binds with high affinity to stem-loop II of U1 RNA. Proc. Natl Acad. Sci. USA, 87, 6393-6397.
38. McCarthy, J. & Kollmus, H. (1995). Cytoplasmic mRNA-protein interactions in eukaryotic gene expression. Trends Biochem. Sci. 20, 191-197.
39. Melese, T. & Xue, Z. (1995). The nucleolus: an organelle formed by the act of building a ribosome. Curr. Opin. Cell Biol. 7, 319-324.
40. Miller, K. G. & 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.
41. Miller, O. L., Jr & Bakken, A. H. (1972). Morphological studies of transcription. In Gene Transcription in Reproductive Tissue (Diczfaly, E., ed.), pp. 155-177, Karolinska Institute, Stockholm.
42. Mougey, E. B., O'Reilly, M., Osheim, Y., Miller, O. L., Beyer, A. & Sollner-Webb, B. (1993). The terminal balls characteristic of eukaryotic rRNA transcription units in chromatin spreads are rRNA processing complexes. Genes Dev. 7, 1609-1619.
43. Nagai, K. & Mattaj, I. W. (1994). In RNA-Protein Interactions (Nagai, K. & Mattaj, I. W., eds), pp. 150-177, IRL Press, Oxford.
44. Nagai, K., Oubridge, C., Jessen, T. H., Li, J. & Evans, P. R. (1990). Crystal structure of the RNA-binding domain of the U1 small nuclear ribonucleoprotein A. Nature, 348, 515-520.
45. Nagai, K., Oudbridge, C., Ito, N., Avis, J. & Evans, P. (1995). The RNP domain: sequence-specific RNA-binding domain involved in processing and transport of RNA. Trends Biochem. Sci. 20, 235-240.
46. Nietfeld, W., Mentzel, H. & Pieler, T. (1990). The Xenopus laevis poly(A) binding protein is composed of multiple functionally independent RNA binding domains. EMBO J. 9, 3699-3705.
47. Olson, M. O. J., Guetzow, K. & Busch, H. (1981). Localization of phosphoprotein C23 in nucleoli by immunological methods. Exp. Cell Res. 135, 259-265.
48. O'Reilly, M. M., French, S. L., Sikes, M. L. & Miller, O. L. (1994). Ultrastructural in situ hybridization to nascent transcripts of highly transcribed rRNA genes in chromatin spreads. Chromosoma, 103, 122-128.
49. Oubridge, C., Ito, N., Evans, P. R., Teo, C.-H. & Nagai, K. (1994). Crystal structure at 1.92 Å resolution of the RNA-binding domain of the U1A spliceosomal protein complexed with an RNA hairpin. Nature, 372, 432-438.
50. r 70,000 protein of the U1 small nuclear ribonucleoprotein particle binds to the 5′ stem-loop of U1 RNA and interact with Sm domain proteins. Proc. Natl Acad. Sci. USA, 85, 747-751.
51. Puvion-Dutilleul, F., Bachellerie, J.-P., Zalta, J.-P. & Bernhard, W. (1977). Morphology of ribosomal transcription units in isolated subnuclear fractions of mammalian cells. Biol Cell 30, 183-194.
52. Query, C. C., Bentley, R. C. & Keene, J. D. (1989a). A specific 31-nucleotide domain of U1 RNA directly interacts with the 70K small nuclear ribonucleoprotein component. Mol. Cell. Biol. 9, 4872-4881.
53. Query, C. C., Bentley, R. C. & Keene, J. D. (1989b). A common RNA recognition motif identified within a defined U1 RNA binding domain of the 70K U1 snRNP protein. Cell, 57, 89-101.
54. Renalier, M. H., Mazan, S., Joseph, N., Michot, B. & Bachellerie, J.-P. (1989). Structure of the 5′ external transcribed spacer of the human ribosomal RNA gene. FEBS Letters, 249, 279-284.
55. Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989). Molecular Cloning 2nd edit., Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
56. Scheer, U. & Weisenberger, D. (1994). The nucleolus. Curr. Opin. Cell. Biol. 6, 354-359.
57. Scherly, D., Boelens, W., van Venrooij, W. J., Dathan, N. A., Hamm, J. & Mattaj, I. W. (1989). Identification of the RNA binding segment of human U1 A protein and definition of its binding site on U1 snRNA. EMBO J. 8, 4163-4170.
58. Scherly, D., Boelens, W., Dathan, N. A., van Venrooij, W. J. & Mattaj, I. W. (1990a). Major determinants of the specificity of interaction between small nuclear ribonucleoproteins U1A and U2B" and their cognate RNAs. Nature, 345, 502-506.
59. Scherly, D., Dathan, N. A., Boelens, W., van Venrooij, W. J. & Mattaj, I. W. (1990b). The U2B" RNP motif as a site of protein-protein interaction. EMBO J. 9, 3675-3681.
60. Tacke, R. & Manley, J. L. (1995). The human splicing factors ASF/SF2 and SC35 possess distinct, functionally significant RNA binding specificities. EMBO J. 14, 3540-3551.
61. Tsai, D. E., Harper, D. S. & Keene, J. D. (1991). U1-snRNP-A protein selects a ten nucleotide consensus sequence from a degenerate RNA pool presented in various structural contexts. Nucl. Acids Res. 19, 4931-4936.
62. Tuerk, C. & Gold, L. (1990). Systematic evolution of ligands by exponential enrichment: RNA ligands to bacteriophage T4 DNA polymerase. Science, 249, 505-510.
63. Tuteja, N., Huang, N. W., Skopac, D., Tuteja, R., Hrvatic, S., Zhang, J., Pongor, S., Joseph, G., Faucher, C., Amalric, F. & Falashi, A. (1995). Human DNA helicase IV is nucleolin, an RNA helicase modulated by phosphorylation. Gene, 160, 143-148.
64. van Gelder, C. W. G., Gunderson, S. I., Jansen, E. J. R., Boelens, W. C., Polycarpou-Scharz, M., Mattaj, I. W. & van Venrooij, W. J. (1993). A complex secondary structure in U1A pre-mRNA that binds two molecules of U1A protein is required for regulation of polyadenylation. EMBO J. 12, 5191-5200.