Splicing factor 2-associated protein p32 participates in ribosome biogenesis by regulating the binding of Nop52 and fibrillarin to preribosome particles

Molecular and Cellular Proteomics

Volumn 10, Issue 8, 2011, Pages

  Yoshikawa, Harunori ^a   Komatsu, Wataru ^a,b,c   Hayano, Toshiya ^a,b,d   Miura, Yutaka ^a,e   Homma, Keiichi ^f   Izumikawa, Keiichi ^h   Ishikawa, Hideaki ^a,e   Miyazawa, Naoki ^a   Tachikawa, Hiroyuki ^a,g   Yamauchi, Yoshio ^h   Isobe, Toshiaki ^b,e,h   Takahashi, Nobuhiro ^a,b,e  

^a TOKYO UNIVERSITY OF AGRICULTURE AND TECHNOLOGY   (Japan)

^b Ministry of Education Culture Sports Science and Technology   (Japan)

^c DOKKYO MEDICAL UNIVERSITY   (Japan)

^d RITSUMEIKAN UNIVERSITY   (Japan)

^e JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^f NATIONAL INSTITUTE OF GENETICS   (Japan)

^g UNIVERSITY OF TOKYO   (Japan)

^h TOKYO METROPOLITAN UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; DNA DIRECTED RNA POLYMERASE III; FIBRILLARIN; PROTEIN P32; RIBOSOME RNA; RNA PRECURSOR; SPLICING FACTOR 2 ASSOCIATED PROTEIN P32; UNCLASSIFIED DRUG; C1QBP PROTEIN, HUMAN; CARRIER PROTEIN; MITOCHONDRIAL PROTEIN; NONHISTONE PROTEIN; NUCLEAR PROTEIN; RNA BINDING PROTEIN; RRP1 PROTEIN, HUMAN;

ALTERNATIVE RNA SPLICING; ARTICLE; BIOGENESIS; HELA CELL; HUMAN; HUMAN CELL; IMMUNOBLOTTING; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; NUCLEOTIDE SEQUENCE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEOMICS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RIBOSOME; RNA INTERFERENCE; UNINDEXED SEQUENCE; BINDING COMPETITION; CELL FRACTIONATION; CELL LINE; COILED BODY; IMMUNOPRECIPITATION; METABOLISM; NUCLEOLUS; PROTEIN BINDING; PROTEIN TRANSPORT; RNA PROCESSING;

BINDING, COMPETITIVE; CARRIER PROTEINS; CELL LINE; CELL NUCLEOLUS; CHROMOSOMAL PROTEINS, NON-HISTONE; COILED BODIES; HUMANS; IMMUNOPRECIPITATION; MITOCHONDRIAL PROTEINS; NUCLEAR PROTEINS; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN TRANSPORT; RIBOSOMES; RNA PRECURSORS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA-BINDING PROTEINS; SUBCELLULAR FRACTIONS;

EID: 80051658722     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M110.006148     Document Type: Article

References (75)

1. Krainer, A. R., Mayeda, A., Kozak, D., and Binns, G. (1991) Functional expression of cloned human splicing factor SF2: homology to RNA binding protein VI 70K, and Drosophila splicing regulators. Cell 66, 383-394 (Pubitemid 121001375)
2. Petersen-Mahrt, S. K., Estmer, C., Ohrmalm, C., Matthews, D. A., Russell, W. C., and Akusjävi, G. (1999) The splicing factor-associated protein, p32, regulates RNA splicing by inhibiting ASF/SF2 RNA binding and phosphorylation. EMBO J. 18, 1014-1024 (Pubitemid 29082280)
3. Mayeda, A., and Krainer, A. R. (1992) Regulation of alternative pre-mRNA splicing by hnRNP A1 and splicing factor SF2. Cell 68, 365-375
4. Mayeda, A., Helfman, D. M., and Krainer, A. R. (1993) Modulation of exon skipping and inclusion by heterogeneous nuclear ribonucleoprotein-A1 and premessenger RNA splicing factor SF2/ASF. Mol. Cell. Biol. 13, 2993-3001 (Pubitemid 23133970)
5. Sun, Q., Mayeda, A., Hampson, R. K., Krainer, A. R., and Rottman, F. M. (1993) General splicing factor SF2/ASF promotes alternative splicing by binding to an exonic splicing enhancer. Genes Dev. 7, 2598-2608 (Pubitemid 24021016)
6. Yang, X., Bani, M. R., Lu, S. J., Rowan, S., Ben-David, Y., and Chabot, B. (1994) The A1 and A1B proteins of heterogeneous nuclear ribonucleoparticles modulate 5′ splice site selection in vivo. Proc. Natl. Acad. Sci. U.S.A. 91, 6924-6928
7. Chabot, B., Blanchette, M., Lapierre, I., and La Branche, H. (1997) An intron element modulating 5′ splice site selection in the hnRNP A1 pre-mRNA interacts with hnRNP A1. Mol. Cell. Biol. 17, 1776-1786 (Pubitemid 27133262)
8. Hanamura, A., Cáceres, J. F., Mayeda, A., Franza, B. R., Jr., and Krainer, A. R. (1998) Regulated tissue-specific expression of antagonistic pre-mRNA splicing factors. RNA 4, 430-444 (Pubitemid 28160784)
9. Jiang, Z. H., Zhang, W. J., Rao, Y., and Wu, J. Y. (1998) Regulation of Ich-1 pre-mRNA alternative splicing and apoptosis by mammalian splicing factors. Proc. Natl. Acad. Sci. U.S.A. 95, 9155-9160
10. Ghebrehiwet, B., Lim, B. L., Peerschke, E. I., Willis, A. C., and Reid, K. B. (1994) Isolation, cDNA cloning, and overexpression of a 33-kD cell surface glycoprotein that binds to the globular 'heads' of C1q. J. Exp. Med. 179, 1809-1821
11. Yadav, G., Prasad, R. L., Jha, B. K., Rai, V., Bhakuni, V., and Datta, K. (2009) Evidence for inhibitory interaction of hyaluronan-binding protein 1 (HABP1/p32/gC1qR) with Streptococcus pneumoniae hyaluronidase. J. Biol. Chem. 284, 3897-3905
12. Deb, T. B., and Datta, K. (1996) Molecular cloning of human fibroblast hyaluronic acid-binding protein confirms its identity with P-32, a protein co-purified with splicing factor SF2. Hyaluronic acid-binding protein as P-32 protein, co-purified with splicing factor SF2. J. Biol. Chem. 271, 2206-2212
13. Chattopadhyay, C., Hawke, D., Kobayashi, R., and Maity, S. N. (2004) Human p32, interacts with B subunit of the CCAAT-binding factor, CBF/NF-Y, and inhibits CBF-mediated transcription activation in vitro. Nucleic Acids Res. 32, 3632-3641 (Pubitemid 39157712)
14. Itahana, K., and Zhang, Y. (2008) Mitochondrial p32 Is a Critical Mediator of ARF-Induced Apoptosis. Cancer Cell 13, 542-553 (Pubitemid 351763900)
15. Sunayama, J., Ando, Y., Itoh, N., Tomiyama, A., Sakurada, K., Sugiyama, A., Kang, D., Tashiro, F., Gotoh, Y., Kuchino, Y., and Kitanaka, C. (2004) Physical and functional interaction between BH3-only protein Hrk and mitochondrial pore-forming protein p32. Cell Death Differ. 11, 771-781 (Pubitemid 39023123)
16. Simos, G., and Georgatos, S. D. (1994) The lamin B receptor-associated protein p34 shares sequence homology and antigenic determinants with the splicing factor 2-associated protein p32. FEBS Lett. 346, 225-228 (Pubitemid 24185609)
17. Bruni, R., and Roizman, B. (1996) Open reading frame P-a herpes simplex virus gene repressed during productive infection encodes a protein that binds a splicing factor and reduces synthesis of viral proteins made from spliced mRNA. Proc. Natl. Acad. Sci. U.S.A. 93, 10423-10427 (Pubitemid 26314638)
18. Matthews, D. A., and Russell, W. C. (1998) Adenovirus core protein V interacts with p32-a protein, which is associated with both the mitochondria and the nucleus. J. Gen. Virol. 79, 1677-1685 (Pubitemid 28330672)
19. Wang, Y., Finan, J. E., Middeldrop, J. M., and Hayward, S. D. (1997) p32/TAP, a cellular protein that interacts with EBNA-1 of Epstein-Barr virus. Virology 236, 18-29 (Pubitemid 27411469)
20. Chen, M. R., Yang, J. F., Wu, C. W., Middeldorp, J. M., and Chen, J. Y. (1998) Physical association between the EBV protein EBNA-1 and p32/TAP/hyaluronectin. J. Biomed. Sci. 5, 173-179 (Pubitemid 28313727)
21. Beatch, M. D., and Hobman, T. C. (2000) Rubella virus capsid associates with host cell protein p32 and localizes to mitochondria. J. Virol. 74, 5569-5576 (Pubitemid 30346591)
22. Luo, Y., Yu, H., and Peterlin, B. M. (1994) Cellular protein modulates effects of human immunodeficiency virus type 1 Rev. J. Virol. 68, 3850-3856 (Pubitemid 24177410)
23. Tange, T. O., Jensen, T. H., and Kjems, J. (1996) In vitro interaction between human immunodeficiency virus type 1 rev protein and splicing factor ASF/SF2-associated protein p32. J. Biol. Chem. 271, 10066-10072 (Pubitemid 26131565)
24. Yu, L., Loewenstein, P. M., Zhang, Z., and Green, M. (1995) In vitro interaction of the human immunodeficiency virus type 1 Tat transactivator and the general transcription factor TFIIB with the cellular protein TAP. J. Virol. 69, 3017-3023
25. Zheng, Y. H., Yu, H. F., and Peterlin, B. M. (2003) Human p32 protein relieves a post-transcriptional block to HIV replication in murine cells. Nat. Cell Biol. 5, 611-618
26. Yanagida, M., Hayano, T., Yamauchi, Y., Shinkawa, T., Natsume, T., Isobe, T., and Takahashi, N. (2004) Human fibrillarin forms a sub-complex with splicing factor 2 associated p32, protein/arginine methyltransferases, tubulin α3 and β1, which is Independent of its association with preribosomal ribonucleoprotein complexes. J. Biol. Chem. 279, 1607-1614 (Pubitemid 38084425)
27. Warner, J. R. (1990) The nucleolus and ribosome formation. Curr. Opin. Cell Biol. 2, 521-527
28. Kiss-László, Z., Henry, Y., Bachellerie, J. P., Caizergues-Ferrer, M., and Kiss, T. (1996) Site-specific ribose methylation of preribosomal RNA: a novel function for small nucleolar RNAs. Cell 85, 1077-1088 (Pubitemid 26231174)
29. Tycowski, K. T., Smith, C. M., Shu, M. D., and Steitz, J. A. (1996) A small nucleolar RNA requirement for site-specific ribose methylation of rRNA in Xenopus. Proc. Natl. Acad. Sci. U.S.A. 93, 14480-14485 (Pubitemid 26418992)
30. Tyc, K., and Steitz, J. A. (1989) U3, U8 and U13 comprise a new class of mammalian snRNPs localized in the cell nucleolus. EMBO J. 8, 3113-3119 (Pubitemid 19275012)
31. Baserga, S. J., Yang, X. D., and Steitz, J. A. (1991) An intact Box C sequence in the U3 snRNA is required for binding of fibrillarin, the protein common to the major family of nucleolar snRNPs. EMBO J. 10, 2645-2651 (Pubitemid 21905741)
32. Aris, J. P., and Blobel, G. (1991) cDNA cloning and sequencing of human fibrillarin, a conserved nucleolar protein recognized by autoimmune antisera. Proc. Natl. Acad. Sci. U.S.A. 88, 931-935 (Pubitemid 21916138)
33. Horsey, E. W., Jakovljevic, J., Miles, T. D., Harnpicharnchai, P., and Woolford, J. L., Jr. (2004) Role of the yeast Rrp1 protein in the dynamics of preribosome maturation. RNA 10, 813-827 (Pubitemid 38529745)
34. Savino, T. M., Bastos, R., Jansen, E., and Hernandez-Verdun, D. (1999) The nucleolar antigen Nop52p, the human homologue of the yeast ribosomal RNA processing RRP1, is recruited at late stages of nucleogenesis. J. Cell Sci. 112, 1889-1900 (Pubitemid 29338814)
35. Savino, T. M., Gébrane-Younès, J., De Mey, J., Sibarita, J. B., and Hernandez-Verdun, D. (2001) Nucleolar Assembly of the rRNA Processing Machinery in Living Cells. J. Cell Biol. 153, 1097-1110 (Pubitemid 34289247)
36. Yanagida, M., Shimamoto, A., Nishikawa, K., Furuichi, Y., Isobe, T., and Takahashi, N. (2001) Isolation and proteomic characterization of the major proteins of the nucleolin-associating ribonucleoprotein complexes. Proteomics 1, 1390-1404 (Pubitemid 33587895)
37. Stavreva, D. A., Kawasaki, M., Dundr, M., Koberna, K., Müller, W. G., Tsujimura-Takahashi, T., Komatsu, W., Hayano, T., Isobe, T., Raska, I., Misteli, T., Takahashi, N., and McNally, J. G. (2006) Potential roles for ubiquitin and the proteasome during ribosome biogenesis. Mol. Cell. Biol. 26, 5131-5145 (Pubitemid 43955825)
38. Watkins, N. J., Lemm, I., Ingelfinger, D., Schneider, C., Hossbach, M., Urlaub, H., and Lührmann, R. (2004) Assembly and maturation of the U3 snoRNP in the nucleoplasm in a large dynamic multiprotein complex. Mol. Cell 16, 789-798 (Pubitemid 39586536)
39. Fujiyama-Nakamura, S., Yoshikawa, H., Homma, K., Hayano, T., Tsujimura-Takahashi, T., Izumikawa, K., Ishikawa, H., Miyazawa, N., Yanagida, M., Miura, M., Shinkawa, T., Yamauchi, Y., Isobe, T., and Takahashi, N. (2009) Parvulin (Par14), a peptidyl prolyl cis-trans isomerase, is a novel rRNA-processing factor that evolved in the metazoan lineage. Mol. Cell. Proteomics 8, 1552-1565
40. Hayano, T., Yanagida, M., Yamauchi, Y., Shinkawa, T., Isobe, T., and Takahashi, N. (2003) Proteomic analysis of human Nop56p-associated preribosomal ribonucleoprotein complexes: Possible link between Nop56p and the nucleolar protein treacle responsible for Treacher Collins syndrome. J. Biol. Chem. 278, 34309-34319 (Pubitemid 37553275)
41. Pestov, D. G., Lapik, Y. R., and Lau, L. F. (2008) Assays for ribosomal RNA processing and ribosome assembly. Curr. Protoc. Cell Biol. 22, Unit 22.11
42. Takahashi, N., and Isobe, T. in Proteomic Biology using LC/MS, Wiley Interscience, John Wiley and Sons Inc., Hoboken NJ U.S.A. (2007) pp. 1-254
43. Even, Y., Durieux, S., Escande, M. L., Lozano, J. C., Peaucellier, G., Weil, D., and Genevière, A. M. (2006) CDC2L5, a Cdk-like kinase with RS domain, interacts with the ASF/SF2-associated protein p32 and affects splicing in vivo, J. Cell. Biochem. 99, 890-904 (Pubitemid 44522007)
44. Crawford, N. P., Yang, H., Mattaini, K. R., and Hunter, K. W. (2009) The metastasis efficiency modifier ribosomal RNA processing 1 homolog B (RRP1B) is a chromatin-associated factor. J. Biol. Chem. 284, 28660-28673
45. Tycowski, K. T., Smith, C. M., Shu, M. D., and Steitz, J. A. (1996) A small nucleolar RNA requirement for site-specific ribose methylation of rRNA in Xenopus. Proc. Natl. Acad. Sci. U.S.A. 93, 14480-14485 (Pubitemid 26418992)
46. Jansen, R. P., Hurt, E. C., Kern, H., Lehtonen, H., Carmo-Fonseca, M., Lapeyre, B., and Tollervey, D. (1991) Evolutionary conservation of the human nucleolar protein fibrillarin and its functional expression in yeast. J. Cell Biol. 113, 715-729 (Pubitemid 21909709)
47. Turner, A. J., Knox, A. A., Prieto, J. L., McStay, B., and Watkins, N. J. (2009) A novel small-subunit processome assembly intermediate that contains the U3 snoRNP, nucleolin, RRP5, and DBP4. Mol. Cell. Biol. 29, 3007-3017
48. Granneman, S., Vogelzangs, J., Lührmann, R., van Venrooij, W. J., Pruijn, G. J., and Watkins, N. J. (2004) Role of pre-rRNA base pairing and 80S complex formation in subnucleolar localization of the U3 snoRNP. Mol. Cell. Biol. 24, 8600-8610 (Pubitemid 39245080)
49. Ginisty, H., Amalric, F., and Bouvet, P. (1998) NCL functions in the first step of ribosomal RNA processing. EMBO J. 17, 1476-1486 (Pubitemid 28105526)
50. Henning, D., So, R. B., Jin, R., Lau, L. F., and Valdez, B. C. (2003) Silencing of RNA helicase II/Guα inhibits mammalian ribosomal RNA production. J. Biol. Chem. 278, 52307-52314 (Pubitemid 38035819)
51. Castle, C. D., Cassimere, E. K., Lee, J., and Denicourt, C. (2010) Las1L is a nucleolar protein required for cell proliferation and ribosome biogenesis. Mol. Cell. Biol. 30, 4404-4414
52. Srivastava, L., Lapik, Y. R., Wang, M., and Pestov, D. G. (2010) Mammalian DEAD box protein Ddx51 acts in 3′ End maturation of 28S rRNA by promoting the release of U8 snoRNA. Mol. Cell. Biol. 30, 2947-2956
53. Eilbracht, J., Reichenzeller, M., Hergt, M., Schnölzer, M., Heid, H., Stöhr, M., Franke, W. W., and Schmidt-Zachmann, M. S. (2004) NO66, a highly conserved dual location protein in the nucleolus and in a special type of synchronously replicating chromatin. Mol. Biol. Cell 15, 1816-1832 (Pubitemid 38401830)
54. Zirwes, R. F., Eilbracht, J., Kneissel, S., and Schmidt-Zachmann, M. S. (2000) A novel helicase-type protein in the nucleolus: protein NOH61. Mol. Biol. Cell 11, 1153-1167 (Pubitemid 30211021)
55. Heindl, K., and Martinez, J. (2010) Nol9 is a novel polynucleotide 5′-kinase involved in ribosomal RNA processing. EMBO J. 29, 4161-4171
56. Haindl, M., Harasim, T., Eick, D., and Muller, S. (2008) The nucleolar SUMO-specific protease SENP3 reverses SUMO modification of nucleophosmin and is required for rRNA processing. EMBO Rep. 9, 273-279 (Pubitemid 351330993)
57. Finkbeiner, E., Haindl, M., and Muller, S. (2011) The SUMO system controls nucleolar partitioning of a novel mammalian ribosome biogenesis complex. EMBO J. 30, 1067-1078
58. Brokstad, K. A., Kalland, K. H., Russell, W. C., and Matthews, D. A. (2001) Mitochondrial protein p32 can accumulate in the nucleus. Biochem. Biophys. Res. Comm. 281, 1161-1169 (Pubitemid 32926742)
59. Izumikawa, K., Yanagida, M., Hayano, T., Tachikawa, H., Komatsu, W., Shimamoto, A., Futami, K., Furuichi, Y., Shinkawa, T., Yamauchi, Y., Isobe, T., and Takahashi, N. (2008) Association of human DNA helicase RecQ5β with RNA polymerase II and its possible role in transcription. Biochem. J. 413, 505-516
60. Fogal, V., Richardson, A. D., Karmali, P. P., Scheffler, I. E., Smith, J. W., and Ruoslahti, E. (2010) Mitochondrial p32 Protein Is a Critical Regulator of Tumor Metabolism via Maintenance of Oxidative Phosphorylation. Mol. Cell. Biol. 30, 1303-1318
61. Takahashi, N., Yanagida, M., Fujiyama, S., Hayano, T., and Isobe, T. (2003) Proteomic snapshot analysis preribosomal ribonucleoprotein complexes formed at various stages of ribosome biogenesis in yeast and mammalian cells. Mass Spectrom. Rev. 22, 287-317
62. Kawasaki, M. (2004) Master's thesis (Isolation and proteomic characterization of the preribosomal ribonucleoprotein complex associated with a novel nucleolar protein-1 that is ubiquitously expressed in human tissue), Graduate School of Agriculture, Tokyo University of Agriculture & Technology
63. Snaar, S., Wiesmeijer, K., Jochemsen, A. G., Tanke, H. J., and Dirks, R. W. (2000) Mutational analysis of fibrillarin and its mobility in living human cells. J. Cell Biol. 151, 653-662
64. Jiang, J., Zhang, Y., Krainer, A. R., and Xu, R. M. (1999) Crystal structure of human p32, a doughnut-shaped acidic mitochondrial matrix protein. Proc. Natl. Acad. Sci. U.S.A. 96, 3572-3577 (Pubitemid 29168951)
65. Seytter, T., Lottspeich, F., Neupert, W., and Schwarz, E. (1998) Mam33p, an oligomeric, acidic protein in the mitochondrial matrix of Saccharomyces cerevisiae is related to the human complement receptor gC1q-R. Yeast14, 303-310 (Pubitemid 28138981)
66. Harnpicharnchai, P., Jakovljevic, J., Horsey, E., Miles, T., Roman, J., Rout, M., Meagher, D., Imai, B., Guo, Y., Brame, C. J., Shabanowitz, J., Hunt, D. F., and Woolford, J. L., Jr. (2001) Composition and functional characterization of yeast 66S ribosome assembly intermediates. Mol. Cell 8, 505-515 (Pubitemid 32946929)
67. Ho, Y., Gruhler, A, Heilbut, A., Bader, G. D., Moore, L., Adams, S. L., Millar, A., Taylor, P., Bennett, K., Boutilier, K., Yang, L., Wolting, C., Donaldson, I., Schandorff, S., Shewnarane, J., Vo, M., Taggart, J., Goudreault, M., Muskat, B., Alfarano, C., Dewar, D., Lin, Z., Michalickova, K., Willems, A. R., Sassi, H., Nielsen, P. A., Rasmussen, K. J., Andersen, J. R., Johansen, L. E., Hansen, L. H., Jespersen, H., Podtelejnikov, A., Nielsen, E., Crawford. J., Poulsen, V., Sørensen, B. D., Matthiesen, J., Hendrickson, R. C., Gleeson, F., Pawson, T., Moran, M. F., Durocher, D., Mann, M., Hogue, C. W., Figeys, D., and Tyers, M. (2002) Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature 415, 180-183 (Pubitemid 34059520)
68. Simonin, D., Diaz, J. J., Massé, T., and Madjar, J. J. (1997) Persistence of ribosomal protein synthesis after infection of HeLa cells by herpes simplex virus type 1. J. Gen. Virol. 78, 435-443 (Pubitemid 27075642)
69. Besse, S., and Puvion-Dutilleul, F. (1996) Intranuclear retention of ribosomal RNAs in response to herpes simplex virus type 1 infection. J. Cell Sci. 109, 119-129 (Pubitemid 26037934)
70. Ponti, D., Troiano, M., Bellenchi, G. C., Battaglia, P. A., and Gigliani, F. (2008) The HIV Tat protein affects processing of ribosomal RNA precursor. BMC Cell Biol. 9, 32
71. Shirai, C., Takai, T., Nariai, M., Horigome, C., and Mizuta, K. (2004) Ebp2p, the yeast homolog of Epstein-Barr virus nuclear antigen 1-binding protein 2, interacts with factors of both the 60 S and the 40 S ribosomal subunit assembly. J. Biol. Chem. 279, 25353-25358 (Pubitemid 38756791)
72. Hiscox, J. A. (2002) The nucleolus-a gateway to viral infection? Arch. Virol. 14, 1077-1089
73. Hiscox, J. A. (2007) RNA viruses: hijacking the dynamic nucleolus. Nat. Rev. Microbiol. 5, 119-127
74. Raychaudhuri, S., Fontanes, V., Barat, B., and Dasgupta, A. (2009) Activation of ribosomal RNA transcription by hepatitis C virus involves upstream binding factor phosphorylation via induction of cyclin D1. Cancer Res. 69, 2057-2064
75. 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 (Pubitemid 23064619)