The ARF Tumor Suppressor Controls Ribosome Biogenesis by Regulating the RNA Polymerase I Transcription Factor TTF-I

Molecular Cell

Volumn 38, Issue 4, 2010, Pages 539-550

  Lessard, Frédéric ^a   Morin, Françoise ^a   Ivanchuk, Stacey ^b,c   Langlois, Frédéric ^a   Stefanovsky, Victor ^a   Rutka, James ^b,c   Moss, Tom ^a  

^a UNIVERSITÉ LAVAL   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c HOSPITAL FOR SICK CHILDREN   (Canada)

Author keywords

DNA; PROTEINS; RNA

Indexed keywords

ARF TUMOR SUPPRESSOR P 14 PROTEIN; ARF TUMOR SUPPRESSOR P 19 PROTEIN; DNA DIRECTED RNA POLYMERASE TRANSCRIPTION FACTOR; NUCLEOPHOSMIN; PROTEIN P53; RIBOSOME RNA; TRANSCRIPTION FACTOR; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; BIOGENESIS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GENE CONTROL; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; NUCLEOLUS; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN TRANSPORT; RIBOSOME BIOGENESIS; RIBOSOME RIBONUCLEIC ACID SYNTHESIS; RNA PROCESSING; RNA SYNTHESIS; SEQUENCE ANALYSIS; TRANSGENE;

ANIMALS; CELL LINE; DNA-BINDING PROTEINS; HELA CELLS; HUMANS; MICE; MICE, INBRED C57BL; NIH 3T3 CELLS; RIBOSOMES; RNA POLYMERASE I; TUMOR SUPPRESSOR PROTEIN P14ARF;

EID: 77952650382     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2010.03.015     Document Type: Article

References (60)

1. Bertwistle D., Sugimoto M., and Sherr C.J. Physical and functional interactions of the Arf tumor suppressor protein with nucleophosmin/B23. Mol. Cell. Biol. 24 (2004) 985-996
2. Carnero A., Hudson J.D., Price C.M., and Beach D.H. p16INK4A and p19ARF act in overlapping pathways in cellular immortalization. Nat. Cell Biol. 2 (2000) 148-155
3. Carrero G., Crawford E., Th'ng J., de Vries G., and Hendzel M.J. Quantification of protein-protein and protein-DNA interactions in vivo, using fluorescence recovery after photobleaching. Methods Enzymol. 375 (2004) 415-442
4. Chen J., Marechal V., and Levine A.J. Mapping of the p53 and mdm-2 interaction domains. Mol. Cell. Biol. 13 (1993) 4107-4114
5. Chen S., Maya-Mendoza A., Zeng K., Tang C.W., Sims P.F., Loric J., and Jackson D.A. Interaction with checkpoint kinase 1 modulates the recruitment of nucleophosmin to chromatin. J. Proteome Res. 8 (2009) 4693-4704
6. Colombo E., Bonetti P., Lazzerini Denchi E., Martinelli P., Zamponi R., Marine J.C., Helin K., Falini B., and Pelicci P.G. Nucleophosmin is required for DNA integrity and p19Arf protein stability. Mol. Cell. Biol. 25 (2005) 8874-8886
7. Colombo E., Martinelli P., Zamponi R., Shing D.C., Bonetti P., Luzi L., Volorio S., Bernard L., Pruneri G., Alcalay M., and Pelicci P.G. Delocalization and destabilization of the Arf tumor suppressor by the leukemia-associated NPM mutant. Cancer Res. 66 (2006) 3044-3050
8. Emmott E., and Hiscox J.A. Nucleolar targeting: the hub of the matter. EMBO Rep. 10 (2009) 231-238
9. Evers R., and Grummt I. Molecular coevolution of mammalian ribosomal gene terminator sequences and the transcription termination factor TTF-I. Proc. Natl. Acad. Sci. USA 92 (1995) 5827-5831
10. Evers R., Smid A., Rudloff U., Lottspeich F., and Grummt I. Different domains of the murine RNA polymerase I-specific termination factor mTTF-I serve distinct functions in transcription termination. EMBO J. 14 (1995) 1248-1256
11. Grisendi S., Bernardi R., Rossi M., Cheng K., Khandker L., Manova K., and Pandolfi P.P. Role of nucleophosmin in embryonic development and tumorigenesis. Nature 437 (2005) 147-153
12. Grisendi S., Mecucci C., Falini B., and Pandolfi P.P. Nucleophosmin and cancer. Nat. Rev. Cancer 6 (2006) 493-505
13. Hahn W.C., and Weinberg R.A. Modelling the molecular circuitry of cancer. Nat. Rev. Cancer 2 (2002) 331-341
14. Hu Q., and Rothblum L.I. TTF-I Isoform 2 (2000), NCBI
15. Huang N., Negi S., Szebeni A., and Olson M.O. Protein NPM3 interacts with the multifunctional nucleolar protein B23/nucleophosmin and inhibits ribosome biogenesis. J. Biol. Chem. 280 (2005) 5496-5502
16. Itahana K., Bhat K.P., Jin A., Itahana Y., Hawke D., Kobayashi R., and Zhang Y. Tumor suppressor ARF degrades B23, a nucleolar protein involved in ribosome biogenesis and cell proliferation. Mol. Cell 12 (2003) 1151-1164
17. Kamijo T., Bodner S., van de Kamp E., Randle D.H., and Sherr C.J. Tumor spectrum in ARF-deficient mice. Cancer Res. 59 (1999) 2217-2222
18. Kelly-Spratt K.S., Gurley K.E., Yasui Y., and Kemp C.J. p19Arf suppresses growth, progression, and metastasis of Hras-driven carcinomas through p53-dependent and -independent pathways. PLoS Biol. 2 (2004) E242
19. Kuhn A., and Grummt I. 3′-end formation of mouse pre-rRNA involves both transcription termination and a specific processing reaction. Genes Dev. 3 (1989) 224-231
20. Kuo M.L., Duncavage E.J., Mathew R., den Besten W., Pei D., Naeve D., Yamamoto T., Cheng C., Sherr C.J., and Roussel M.F. Arf induces p53-dependent and -independent antiproliferative genes. Cancer Res. 63 (2003) 1046-1053
21. Längst G., Becker P.B., and Grummt I. TTF-I determines the chromatin architecture of the active rDNA promoter. EMBO J. 17 (1998) 3135-3145
22. Lechertier T., Sirri V., Hernandez-Verdun D., and Roussel P. A B23-interacting sequence as a tool to visualize protein interactions in a cellular context. J. Cell Sci. 120 (2007) 265-275
23. Léotoing L., Meunier L., Manin M., Mauduit C., Decaussin M., Verrijdt G., Claessens F., Benahmed M., Veyssière G., Morel L., and Beaudoin C. Influence of nucleophosmin/B23 on DNA binding and transcriptional activity of the androgen receptor in prostate cancer cell. Oncogene 27 (2008) 2858-2867
24. Levine A.J., Hu W., and Feng Z. The P53 pathway: what questions remain to be explored?. Cell Death Differ. 13 (2006) 1027-1036
25. Li Y.P., Busch R.K., Valdez B.C., and Busch H. C23 interacts with B23, a putative nucleolar-localization-signal-binding protein. Eur. J. Biochem. 237 (1996) 153-158
26. Lim M.J., and Wang X.W. Nucleophosmin and human cancer. Cancer Detect. Prev. 30 (2006) 481-490
27. Lindström M.S., and Zhang Y. B23 and ARF: friends or foes?. Cell Biochem. Biophys. 46 (2006) 79-90
28. Lindström M.S., and Zhang Y. Ribosomal protein S9 is a novel B23/NPM-binding protein required for normal cell proliferation. J. Biol. Chem. 283 (2008) 15568-15576
29. Liu Y., Riley L.B., Bohn S.A., Boice J.A., Stadler P.B., and Sherley J.L. Comparison of bax, waf1, and IMP dehydrogenase regulation in response to wild-type p53 expression under normal growth conditions. J. Cell. Physiol. 177 (1998) 364-376
30. Llanos S., Clark P.A., Rowe J., and Peters G. Stabilization of p53 by p14ARF without relocation of MDM2 to the nucleolus. Nat. Cell Biol. 3 (2001) 445-452
31. Lohrum M.A., Ashcroft M., Kubbutat M.H., and Vousden K.H. Identification of a cryptic nucleolar-localization signal in MDM2. Nat. Cell Biol. 2 (2000) 179-181
32. Luthman H., and Magnusson G. High efficiency polyoma DNA transfection of chloroquine treated cells. Nucleic Acids Res. 11 (1983) 1295-1308
33. Maggi Jr. L.B., Kuchenruether M., Dadey D.Y., Schwope R.M., Grisendi S., Townsend R.R., Pandolfi P.P., and Weber J.D. Nucleophosmin serves as a rate-limiting nuclear export chaperone for the Mammalian ribosome. Mol. Cell. Biol. 28 (2008) 7050-7065
34. Mason S.W., Wallisch M., and Grummt I. RNA polymerase I transcription termination: similar mechanisms are employed by yeast and mammals. J. Mol. Biol. 268 (1997) 229-234
35. Moss T., Langlois F., Gagnon-Kugler T., and Stefanovsky V. A housekeeper with power of attorney: the rRNA genes in ribosome biogenesis. Cell. Mol. Life Sci. 64 (2007) 29-49
36. Muramatsu M., Smetana K., and Busch H. Quantitative Aspects of Isolation of Nucleoli of the Walker Carcinosarcoma and Liver of the Rat. Cancer Res. 23 (1963) 510-518
37. Naoe T., Suzuki T., Kiyoi H., and Urano T. Nucleophosmin: a versatile molecule associated with hematological malignancies. Cancer Sci. 97 (2006) 963-969
38. Németh A., Strohner R., Grummt I., and Längst G. The chromatin remodeling complex NoRC and TTF-I cooperate in the regulation of the mammalian rRNA genes in vivo. Nucleic Acids Res. 32 (2004) 4091-4099
39. Okuwaki M., Iwamatsu A., Tsujimoto M., and Nagata K. Identification of Nucleophosmin/B23, an acidic nucleolar protein, as a stimulatory factor for in vitro replication of adenovirus DNA complexed with viral basic core proteins. J. Mol. Biol. 311 (2001) 41-55
40. Palaniswamy V., Moraes K.C., Wilusz C.J., and Wilusz J. Nucleophosmin is selectively deposited on mRNA during polyadenylation. Nat. Struct. Mol. Biol. 13 (2006) 429-435
41. Percipalle P., Fomproix N., Cavellan E., Voit R., Reimer G., Kruger T., Thyberg J., Scheer U., Grummt I., and Ostlund Farrants A.K. The chromatin remodelling complex WSTF-SNF2h interacts with nuclear myosin 1 and has a role in RNA polymerase I transcription. EMBO Rep. 7 (2006) 525-530
42. Rodway H., Llanos S., Rowe J., and Peters G. Stability of nucleolar versus non-nucleolar forms of human p14(ARF). Oncogene 23 (2004) 6186-6192
43. Sander E.E., Mason S.W., Munz C., and Grummt I. The amino-terminal domain of the transcription termination factor TTF-I causes protein oligomerization and inhibition of DNA binding. Nucleic Acids Res. 24 (1996) 3677-3684
44. Savkur R.S., and Olson M.O. Preferential cleavage in pre-ribosomal RNA byprotein B23 endoribonuclease. Nucleic Acids Res. 26 (1998) 4508-4515
45. Schneider D.A., Michel A., Sikes M.L., Vu L., Dodd J.A., Salgia S., Osheim Y.N., Beyer A.L., and Nomura M. Transcription elongation by RNA polymerase I is linked to efficient rRNA processing and ribosome assembly. Mol. Cell 26 (2007) 217-229
46. Sharpless N.E. INK4a/ARF: a multifunctional tumor suppressor locus. Mutat. Res. 576 (2005) 22-38
47. Sherr C.J. Divorcing ARF and p53: an unsettled case. Nat. Rev. Cancer 6 (2006) 663-673
48. Stefanovsky V.Y., Pelletier G., Hannan R., Gagnon-Kugler T., Rothblum L.I., and Moss T. An immediate response of ribosomal transcription to growth factor stimulation in mammals is mediated by ERK phosphorylation of UBF. Mol. Cell 8 (2001) 1063-1073
49. Stefanovsky V.Y., Langlois F., Gagnon-Kugler T., Rothblum L.I., and Moss T. Growth factor signaling regulates elongation of RNA polymerase I transcription in mammals via UBF phosphorylation and r-chromatin remodeling. Mol. Cell 21 (2006) 629-639
50. Strohner R., Nemeth A., Jansa P., Hofmann-Rohrer U., Santoro R., Längst G., and Grummt I. NoRC-a novel member of mammalian ISWI-containing chromatin remodeling machines. EMBO J. 20 (2001) 4892-4900
51. Strohner R., Németh A., Nightingale K.P., Grummt I., Becker P.B., and Längst G. Recruitment of the nucleolar remodeling complex NoRC establishes ribosomal DNA silencing in chromatin. Mol. Cell. Biol. 24 (2004) 1791-1798
52. Sugimoto M., Kuo M.L., Roussel M.F., and Sherr C.J. Nucleolar Arf tumor suppressor inhibits ribosomal RNA processing. Mol. Cell 11 (2003) 415-424
53. Szebeni A., and Olson M.O.J. Nucleolar protein B23 has molecular chaperone activities. Protein Sci. 8 (1999) 905-912
54. Szebeni A., Hingorani K., Negi S., and Olson M.O. Role of protein kinase CK2 phosphorylation in the molecular chaperone activity of nucleolar protein b23. J. Biol. Chem. 278 (2003) 9107-9115
55. Tschochner H., and Hurt E. Pre-ribosomes on the road from the nucleolus to the cytoplasm. Trends Cell Biol. 13 (2003) 255-263
56. Vousden K.H., and Lu X. Live or let die: the cell's response to p53. Nat. Rev. Cancer 2 (2002) 594-604
57. Weber J.D., Jeffers J.R., Rehg J.E., Randle D.H., Lozano G., Roussel M.F., Sherr C.J., and Zambetti G.P. p53-independent functions of the p19(ARF) tumor suppressor. Genes Dev. 14 (2000) 2358-2365
58. Weber J.D., Taylor L.J., Roussel M.F., Sherr C.J., and Bar-Sagi D. Nucleolar Arf sequesters Mdm2 and activates p53. Nat. Cell Biol. 1 (1999) 20-26
59. Xu J. Preparation, culture, and immortalization of mouse embryonic fibroblasts. Curr. Protoc. Mol. Biol. 28 (2005) Unit 28.1
60. Zhang Y. The ARF-B23 connection: implications for growth control and cancer treatment. Cell Cycle 3 (2004) 259-262