Importin 7 and exportin 1 Link c-Myc and p53 to regulation of ribosomal Biogenesis

Molecular Cell

Volumn 45, Issue 2, 2012, Pages 222-232

  Golomb, Lior ^a   Bublik, Debora Rosa ^a   Wilder, Sylvia ^a   Nevo, Reinat ^a   Kiss, Vladimir ^a   Grabusic, Kristina ^b   Volarevic, Sinisa ^b   Oren, Moshe ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b UNIVERSITY OF RIJEKA   (Croatia)

Author keywords

[No Author keywords available]

Indexed keywords

EXPORTIN 1; IMPORTIN 7; KARYOPHERIN BETA; MYC PROTEIN; PROTEIN MDM2; PROTEIN P53; RIBOSOME PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BIOGENESIS; CELL CYCLE ARREST; CELL STRESS; GENE ACTIVATION; GENE OVEREXPRESSION; GENE SILENCING; HUMAN; PROTEIN BINDING; PROTEIN DEPLETION; RIBOSOME; TRANSCRIPTION REGULATION;

ACTIVE TRANSPORT, CELL NUCLEUS; CELL LINE, TUMOR; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; KARYOPHERINS; PROTO-ONCOGENE PROTEINS C-MYC; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RIBOSOMAL PROTEINS; RIBOSOMES; STRESS, PHYSIOLOGICAL; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84856286957     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2011.11.022     Document Type: Article

References (71)

1. Barkic M., Crnomarkovic S., Grabusic K., Bogetic I., Panic L., Tamarut S., Cokaric M., Jeric I., Vidak S., Volarevic S. The p53 tumor suppressor causes congenital malformations in Rpl24-deficient mice and promotes their survival. Mol. Cell. Biol. 2009, 29:2489-2504.
2. Boisvert F.M., Lamond A.I. p53-dependent subcellular proteome localization following DNA damage. Proteomics 2010, 10:4087-4097.
3. Boulon S., Westman B.J., Hutten S., Boisvert F.M., Lamond A.I. The nucleolus under stress. Mol. Cell 2010, 40:216-227.
4. Brady S.N., Yu Y., Maggi L.B., Weber J.D. ARF impedes NPM/B23 shuttling in an Mdm2-sensitive tumor suppressor pathway. Mol. Cell. Biol. 2004, 24:9327-9338.
5. Budde A., Grummt I. p53 represses ribosomal gene transcription. Oncogene 1999, 18:1119-1124.
6. Burger K., Muhl B., Harasim T., Rohrmoser M., Malamoussi A., Orban M., Kellner M., Gruber-Eber A., Kremmer E., Holzel M., Eick D. Chemotherapeutic drugs inhibit ribosome biogenesis at various levels. J.Biol. Chem. 2010, 285:12416-12425.
7. Choong M.L., Yang H., Lee M.A., Lane D.P. Specific activation of the p53 pathway by low dose actinomycin D: a new route to p53 based cyclotherapy. Cell Cycle 2009, 8:2810-2818.
8. Cohen A.A., Geva-Zatorsky N., Eden E., Frenkel-Morgenstern M., Issaeva I., Sigal A., Milo R., Cohen-Saidon C., Liron Y., Kam Z., et al. Dynamic proteomics of individual cancer cells in response to a drug. Science 2008, 322:1511-1516.
9. Dai M.S., Lu H. Inhibition of MDM2-mediated p53 ubiquitination and degradation by ribosomal protein L5. J.Biol. Chem. 2004, 279:44475-44482.
10. Dai M.S., Zeng S.X., Jin Y., Sun X.X., David L., Lu H. Ribosomal protein L23 activates p53 by inhibiting MDM2 function in response to ribosomal perturbation but not to translation inhibition. Mol. Cell. Biol. 2004, 24:7654-7668.
11. Eilers M., Eisenman R.N. Myc's broad reach. Genes Dev. 2008, 22:2755-2766.
12. Fassati A., Gorlich D., Harrison I., Zaytseva L., Mingot J.M. Nuclear import of HIV-1 intracellular reverse transcription complexes is mediated by importin 7. EMBO J. 2003, 22:3675-3685.
13. Freedman D.A., Levine A.J. Nuclear export is required for degradation of endogenous p53 by MDM2 and human papillomavirus E6. Mol. Cell. Biol. 1998, 18:7288-7293.
14. Fumagalli S., Di Cara A., Neb-Gulati A., Natt F., Schwemberger S., Hall J., Babcock G.F., Bernardi R., Pandolfi P.P., Thomas G. Absence of nucleolar disruption after impairment of 40S ribosome biogenesis reveals an rpL11-translation-dependent mechanism of p53 induction. Nat. Cell Biol. 2009, 11:501-508.
15. Gomez-Roman N., Grandori C., Eisenman R.N., White R.J. Direct activation of RNA polymerase III transcription by c-Myc. Nature 2003, 421:290-294.
16. Gottifredi V., Karni-Schmidt O., Shieh S.S., Prives C. p53 down-regulates CHK1 through p21 and the retinoblastoma protein. Mol. Cell. Biol. 2001, 21:1066-1076.
17. Grandori C., Gomez-Roman N., Felton-Edkins Z.A., Ngouenet C., Galloway D.A., Eisenman R.N., White R.J. c-Myc binds to human ribosomal DNA and stimulates transcription of rRNA genes by RNA polymerase I. Nat. Cell Biol. 2005, 7:311-318.
18. Greco A. Involvement of the nucleolus in replication of human viruses. Rev. Med. Virol. 2009, 19:201-214.
19. Gustafson W.C., Weiss W.A. Myc proteins as therapeutic targets. Oncogene 2010, 29:1249-1259.
20. He T.C., Sparks A.B., Rago C., Hermeking H., Zawel L., da Costa L.T., Morin P.J., Vogelstein B., Kinzler K.W. Identification of c-MYC as a target of the APC pathway. Science 1998, 281:1509-1512.
21. Jakel S., Gorlich D. Importin beta, transportin, RanBP5 and RanBP7 mediate nuclear import of ribosomal proteins in mammalian cells. EMBO J. 1998, 17:4491-4502.
22. Jakel S., Albig W., Kutay U., Bischoff F.R., Schwamborn K., Doenecke D., Gorlich D. The importin beta/importin 7 heterodimer is a functional nuclear import receptor for histone H1. EMBO J. 1999, 18:2411-2423.
23. Jakel S., Mingot J.M., Schwarzmaier P., Hartmann E., Gorlich D. Importins fulfil a dual function as nuclear import receptors and cytoplasmic chaperones for exposed basic domains. EMBO J. 2002, 21:377-386.
24. Jin A., Itahana K., O'Keefe K., Zhang Y. Inhibition of HDM2 and activation of p53 by ribosomal protein L23. Mol. Cell. Biol. 2004, 24:7669-7680.
25. Johnson A.W., Lund E., Dahlberg J. Nuclear export of ribosomal subunits. Trends Biochem. Sci. 2002, 27:580-585.
26. Kondoh N., Shuda M., Tanaka K., Wakatsuki T., Hada A., Yamamoto M. Enhanced expression of S8, L12, L23a, L27 and L30 ribosomal protein mRNAs in human hepatocellular carcinoma. Anticancer Res. 2001, 21:2429-2433.
27. Kuroda M., Oikawa K., Yoshida K., Takeuchi A., Takeuchi M., Usui M., Umezawa A., Mukai K. Effects of 3-methylcholanthrene on the transcriptional activity and mRNA accumulation of the oncogene hWAPL. Cancer Lett. 2005, 221:21-28.
28. Lam Y.W., Lamond A.I., Mann M., Andersen J.S. Analysis of nucleolar protein dynamics reveals the nuclear degradation of ribosomal proteins. Curr. Biol. 2007, 17:749-760.
29. Li S.R., Gyselman V.G., Dorudi S., Bustin S.A. Elevated levels of RanBP7 mRNA in colorectal carcinoma are associated with increased proliferation and are similar to the transcription pattern of the proto-oncogene c-myc. Biochem. Biophys. Res. Commun. 2000, 271:537-543.
30. Lim M.J., Wang X.W. Nucleophosmin and human cancer. Cancer Detect. Prev. 2006, 30:481-490.
31. Lindstrom M.S., Nister M. Silencing of ribosomal protein S9 elicits a multitude of cellular responses inhibiting the growth of cancer cells subsequent to p53 activation. PLoS ONE 2010, 5:e9578. 10.1371/journal.pone.0009578.
32. Lohrum M.A., Ludwig R.L., Kubbutat M.H., Hanlon M., Vousden K.H. Regulation of HDM2 activity by the ribosomal protein L11. Cancer Cell 2003, 3:577-587.
33. Maggi L.B., Kuchenruether M., Dadey D.Y., Schwope R.M., Grisendi S., Townsend R.R., Pandolfi P.P., Weber J.D. Nucleophosmin serves as a rate-limiting nuclear export chaperone for the Mammalian ribosome. Mol. Cell. Biol. 2008, 28:7050-7065.
34. Marechal V., Elenbaas B., Piette J., Nicolas J.C., Levine A.J. The ribosomal L5 protein is associated with mdm-2 and mdm-2-p53 complexes. Mol. Cell. Biol. 1994, 14:7414-7420.
35. Montanaro L., Trere D., Derenzini M. Nucleolus, ribosomes, and cancer. Am. J. Pathol. 2008, 173:301-310.
36. Naora H., Takai I., Adachi M., Naora H. Altered cellular responses by varying expression of a ribosomal protein gene: sequential coordination of enhancement and suppression of ribosomal protein S3a gene expression induces apoptosis. J.Cell Biol. 1998, 141:741-753.
37. Nelson J.D., Denisenko O., Bomsztyk K. Protocol for the fast chromatin immunoprecipitation (ChIP) method. Nat. Protoc. 2006, 1:179-185.
38. Neville M., Stutz F., Lee L., Davis L.I., Rosbash M. The importin-beta family member Crm1p bridges the interaction between Rev and the nuclear pore complex during nuclear export. Curr. Biol. 1997, 7:767-775.
39. Panic L., Tamarut S., Sticker-Jantscheff M., Barkic M., Solter D., Uzelac M., Grabusic K., Volarevic S. Ribosomal protein S6 gene haploinsufficiency is associated with activation of a p53-dependent checkpoint during gastrulation. Mol. Cell. Biol. 2006, 26:8880-8891.
40. Plafker S.M., Macara I.G. Ribosomal protein L12 uses a distinct nuclear import pathway mediated by importin 11. Mol. Cell. Biol. 2002, 22:1266-1275.
41. Pogue-Geile K., Geiser J.R., Shu M., Miller C., Wool I.G., Meisler A.I., Pipas J.M. Ribosomal protein genes are overexpressed in colorectal cancer: isolation of a cDNA clone encoding the human S3 ribosomal protein. Mol. Cell. Biol. 1991, 11:3842-3849.
42. Qi Y., Gregory M.A., Li Z., Brousal J.P., West K., Hann S.R. p19ARF directly and differentially controls the functions of c-Myc independently of p53. Nature 2004, 431:712-717.
43. Roth J., Dobbelstein M., Freedman D.A., Shenk T., Levine A.J. Nucleo-cytoplasmic shuttling of the hdm2 oncoprotein regulates the levels of the p53 protein via a pathway used by the human immunodeficiency virus rev protein. EMBO J. 1998, 17:554-564.
44. Rout M.P., Blobel G., Aitchison J.D. A distinct nuclear import pathway used by ribosomal proteins. Cell 1997, 89:715-725.
45. Rubbi C.P., Milner J. Disruption of the nucleolus mediates stabilization of p53 in response to DNA damage and other stresses. EMBO J. 2003, 22:6068-6077.
46. Ruggero D., Pandolfi P.P. Does the ribosome translate cancer?. Nat. Rev. Cancer 2003, 3:179-192.
47. Ruggero D., Grisendi S., Piazza F., Rego E., Mari F., Rao P.H., Cordon-Cardo C., Pandolfi P.P. Dyskeratosis congenita and cancer in mice deficient in ribosomal RNA modification. Science 2003, 299:259-262.
48. Saijou E., Itoh T., Kim K.W., Iemura S., Natsume T., Miyajima A. Nucleocytoplasmic shuttling of the zinc finger protein EZI Is mediated by importin-7-dependent nuclear import and CRM1-independent export mechanisms. J.Biol. Chem. 2007, 282:32327-32337.
49. Schatz O., Oft M., Dascher C., Schebesta M., Rosorius O., Jaksche H., Dobrovnik M., Bevec D., Hauber J. Interaction of the HIV-1 rev cofactor eukaryotic initiation factor 5A with ribosomal protein L5. Proc. Natl. Acad. Sci. USA 1998, 95:1607-1612.
50. Shats I., Milyavsky M., Tang X., Stambolsky P., Erez N., Brosh R., Kogan I., Braunstein I., Tzukerman M., Ginsberg D., Rotter V. p53-dependent down-regulation of telomerase is mediated by p21waf1. J.Biol. Chem. 2004, 279:50976-50985.
51. Shen A., Wang Y., Zhao Y., Zou L., Sun L., Cheng C. Expression of CRM1 in human gliomas and its significance in p27 expression and clinical prognosis. Neurosurgery 2009, 65:153-159. discussion 159-160.
52. Smith E.R., Cai K.Q., Smedberg J.L., Ribeiro M.M., Rula M.E., Slater C., Godwin A.K., Xu X.X. Nuclear entry of activated MAPK is restricted in primary ovarian and mammary epithelial cells. PLoS ONE 2010, 5:e9295. 10.1371/journal.pone.0009295.
53. Sun X.X., Wang Y.G., Xirodimas D.P., Dai M.S. Perturbation of 60S ribosomal biogenesis results in ribosomal protein L5- and L11-dependent p53 activation. J.Biol. Chem. 2010, 285:25812-25821.
54. Tao W., Levine A.J. P19(ARF) stabilizes p53 by blocking nucleo-cytoplasmic shuttling of Mdm2. Proc. Natl. Acad. Sci. USA 1999, 96:6937-6941.
55. Thomas F., Kutay U. Biogenesis and nuclear export of ribosomal subunits in higher eukaryotes depend on the CRM1 export pathway. J.Cell Sci. 2003, 116:2409-2419.
56. Turner J.G., Sullivan D.M. CRM1-mediated nuclear export of proteins and drug resistance in cancer. Curr. Med. Chem. 2008, 15:2648-2655.
57. van der Watt P.J., Maske C.P., Hendricks D.T., Parker M.I., Denny L., Govender D., Birrer M.J., Leaner V.D. The Karyopherin proteins, Crm1 and Karyopherin beta1, are overexpressed in cervical cancer and are critical for cancer cell survival and proliferation. Int. J. Cancer 2009, 124:1829-1840.
58. van der Watt P.J., Leaner V.D. The nuclear exporter, Crm1, is regulated by NFY and Sp1 in cancer cells and repressed by p53 in response to DNA damage. Biochim. Biophys. Acta. 2011, 1809:316-326.
59. van Riggelen J., Yetil A., Felsher D.W. MYC as a regulator of ribosome biogenesis and protein synthesis. Nat. Rev. Cancer 2010, 10:301-309.
60. Wang B., Xiao Z., Ren E.C. Redefining the p53 response element. Proc. Natl. Acad. Sci. USA 2009, 106:14373-14378.
61. Wang B., Xiao Z., Ko H.L., Ren E.C. The p53 response element and transcriptional repression. Cell Cycle 2010, 9:870-879.
62. Warner J.R., Mitra G., Schwindinger W.F., Studeny M., Fried H.M. Saccharomyces cerevisiae coordinates accumulation of yeast ribosomal proteins by modulating mRNA splicing, translational initiation, and protein turnover. Mol. Cell. Biol. 1985, 5:1512-1521.
63. Wu C.H., Sahoo D., Arvanitis C., Bradon N., Dill D.L., Felsher D.W. Combined analysis of murine and human microarrays and ChIP analysis reveals genes associated with the ability of MYC to maintain tumorigenesis. PLoS Genet. 2008, 4:e1000090. 10.1371/journal.pgen.1000090.
64. Yadavilli S., Mayo L.D., Higgins M., Lain S., Hegde V., Deutsch W.A. Ribosomal protein S3: A multi-functional protein that interacts with both p53 and MDM2 through its KH domain. DNA Repair (Amst.) 2009, 8:1215-1224.
65. Yu Y., Maggi L.B., Brady S.N., Apicelli A.J., Dai M.S., Lu H., Weber J.D. Nucleophosmin is essential for ribosomal protein L5 nuclear export. Mol. Cell. Biol. 2006, 26:3798-3809.
66. Yuan X., Zhou Y., Casanova E., Chai M., Kiss E., Grone H.J., Schutz G., Grummt I. Genetic inactivation of the transcription factor TIF-IA leads to nucleolar disruption, cell cycle arrest, and p53-mediated apoptosis. Mol. Cell 2005, 19:77-87.
67. Zaitseva L., Cherepanov P., Leyens L., Wilson S.J., Rasaiyaah J., Fassati A. HIV-1 exploits importin 7 to maximize nuclear import of its DNA genome. Retrovirology 2009, 6:11.
68. Zeller K.I., Haggerty T.J., Barrett J.F., Guo Q., Wonsey D.R., Dang C.V. Characterization of nucleophosmin (B23) as a Myc target by scanning chromatin immunoprecipitation. J.Biol. Chem. 2001, 276:48285-48291.
69. Zhang Y., Lu H. Signaling to p53: ribosomal proteins find their way. Cancer Cell 2009, 16:369-377.
70. Zhu Y., Poyurovsky M.V., Li Y., Biderman L., Stahl J., Jacq X., Prives C. Ribosomal protein S7 is both a regulator and a substrate of MDM2. Mol. Cell 2009, 35:316-326.
71. Zindy F., Eischen C.M., Randle D.H., Kamijo T., Cleveland J.L., Sherr C.J., Roussel M.F. Myc signaling via the ARF tumor suppressor regulates p53-dependent apoptosis and immortalization. Genes Dev. 1998, 12:2424-2433.