Ribosomal protein L23 activates p53 by inhibiting MDM2 function in response to ribosomal perturbation but not to translation inhibition

Molecular and Cellular Biology

Volumn 24, Issue 17, 2004, Pages 7654-7668

  Dai, Mu Shui ^a   Zeng, Shelya X ^a   Jin, Yetao ^a   Sun, Xiao Xin ^a   David, Larry ^b   Lu, Hua ^a,b  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DACTINOMYCIN; PROTEIN MDM2; PROTEIN P53; RIBOSOME PROTEIN; RIBOSOME PROTEIN L23; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANTIBODY AFFINITY; ARTICLE; CELL CYCLE G1 PHASE; CELL GROWTH; CELL STRAIN SAOS 2; CELL STRAIN U 2 OS; COMPLEX FORMATION; CONTROLLED STUDY; EMBRYO; FEEDBACK SYSTEM; GAMMA IRRADIATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; RIBOSOME; TRANSLATION REGULATION;

AMINO ACID SEQUENCE; CELL CYCLE; CELL LINE; DACTINOMYCIN; GAMMA RAYS; HUMANS; MACROMOLECULAR SUBSTANCES; NUCLEAR PROTEINS; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; PROTEIN SYNTHESIS INHIBITORS; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-MDM2; RIBOSOMAL PROTEINS; RIBOSOMES; RNA, SMALL INTERFERING; TUMOR SUPPRESSOR PROTEIN P53;

EID: 4344685939     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.24.17.7654-7668.2004     Document Type: Article

References (77)

1. Ashcroft, M., M. H. Kubbutat, and K. H. Vousden. 1999. Regulation of p53 function and stability by phosphorylation. Mol. Cell. Biol. 19:1751-1758.
2. Ashcroft, M., Y. Taya, and K. H. Vousden. 2000. Stress signals utilize multiple pathways to stabilize p53. Mol. Cell. Biol. 20:3224-3233.
3. Banin, S., L. Moyal, S. Shieh, Y. Taya, C. W. Anderson, L. Chessa, N. I. Smorodinsky, C. Prives, Y. Reiss, Y. Shiloh, and Y. Ziv. 1998. Enhanced phosphorylation of p53 by ATM in response to DNA damage. Science 281:1674-1677.
4. Barak, Y., T. Juven, R. Haffner, and M. Oren. 1993. mdm2 expression is induced by wild type p53 activity. EMBO J. 12:461-468.
5. Boyd, M. T., N. Vlatkovic, and D. S. Haines. 2000. A novel cellular protein (MTBP) binds to MDM2 and induces a G1 arrest that is suppressed by MDM2. J. Biol. Chem. 275:31883-31890.
6. Boyd, S. D., K. Y. Tsai, and T. Jacks. 2000. An intact HDM2 RING-finger domain is required for nuclear exclusion of p53. Nat. Cell Biol. 2:563-568.
7. Budde, A., and I. Grummt. 1999. p53 represses ribosomal gene transcription. Oncogene 18:1119-1124.
8. Canman, C. E., D. S. Lim, K. A. Cimprich, Y. Taya, K. Tamai, K. Sakaguchi, E. Appella, M. B. Kastan, and J. D. Siliciano. 1998. Activation of the ATM kinase by ionizing radiation and phosphorylation of p53. Science 281:1677-1679.
9. Cavanaugh, A. H., W. M. Hempel, L. J. Taylor, V. Rogalsky, G. Todorov, and L. I. Rothblum. 1995. Activity of RNA polymerase I transcription factor UBF blocked by Rb gene product. Nature 374:177-180.
10. Chen, J., V. Marechal, and A. J. Levine. 1993. Mapping of the p53 and mdm-2 interaction domains. Mol. Cell. Biol. 13:4107-4114.
11. Ciarmatori, S., P. H. Scott, J. E. Sutcliffe, A, McLees, H. M. Alzuherri, J. H. Dannenberg, H. te Riele, I. Grummt, R. Voit, and R. J. White. 2001. Overlapping functions of the pRb family in the regulation of rRNA synthesis. Mol. Cell. Biol. 21:5806-5814.
12. Dignam, J. D., R. M. Lebovitz, and R. G. Roeder. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11:1475-1489.
13. Draptchinskaia, N., P. Gustavsson, B. Andersson, M. Pettersson, T. N. Willig, I. Dianzani, S. Ball, G. Tchernia, J. Klar, H. Matsson, D. Tentler, N. Mohandas, B. Carlsson, and N. Dahl. 1999. The gene encoding ribosomal protein S19 is mutated in Diamond-Blackfan anaemia. Nat. Genet. 21:169-175.
14. Eichler, D. C., and N. Craig. 1994. Processing of eukaryotic ribosomal RNA. Prog. Nucleic Acid Res. Mol. Biol. 49:197-239.
15. Elenbaas, B., M. Dobbelstein, J. Roth, T. Shenk, and A. J. Levine. 1996. The MDM2 oncoprotein binds specifically to RNA through its RING finger domain. Mol. Med. 2:439-451.
16. Fang, S., J. P. Jensen, R. L. Ludwig, K. H. Vousden, and A. M. Weissman. 2000. Mdm2 is a RING finger-dependent ubiquitin protein ligase for itself and p53. J. Biol. Chem. 275:8945-8951.
17. Feng, Y., D. Absher, D. E. Eberhart, V. Brown, H. E. Malter, and S. T. Warren. 1997. FMRP associates with polyribosomes as an mRNP, and the I304N mutation of severe fragile X syndrome abolishes this association. Mol. Cell 1:109-118.
18. Geyer, R. K., Z. K. Yu, and C. G. Maki. 2000. The MDM2 RING-finger domain is required to promote p53 nuclear export. Nat. Cell Biol. 2:569-573.
19. Gu, J., H. Kawal, L. Nie, H. Kitao, D. Wiederschain, A. G. Jochemsen, J. Parant, G. Lozano, and Z. M. Yuan. 2002. Mutual dependence of MDM2 and MDMX in their functional inactivation of p53. J. Biol. Chem. 277:19251-19254.
20. Haupt, Y., R. Maya, A. Kazaz, and M. Oren. 1997. Mdm2 promotes the rapid degradation of p53. Nature 387:296-299.
21. Honda, R., H. Tanaka, and H. Yasuda. 1997. Oncoprotein MDM2 is a ubiquitin ligase E3 for tumor suppressor p53. FEBS Lett. 420:25-27.
22. Honda, R., and H. Yasuda. 1999. Association of p19(ARF) with Mdm2 inhibits ubiquitin ligase activity of Mdm2 for tumor suppressor p53. EMBO J. 18:22-27.
23. Iordanov, M. S., D. Pribnow, J. L. Magun, T. H. Dinh, J. A. Pearson, S. L. Chen, and B. E. Magun. 1997. Ribotoxic stress response: activation of the stress-activated protein kinase JNK1 by inhibitors of the peptidyl transferase reaction and by sequence-specific RNA damage to the alpha-sarcin/ricin loop in the 28S rRNA. Mol. Cell. Biol. 17:3373-3381.
24. Jackson, M. W., and S. J. Berberich. 2000. MdmX protects p53 from Mdm2-mediated degradation. Mol. Cell. Biol. 20:1001-1007.
25. Jin, Y., H. Lee, S. X. Zeng, M. S. Dai, and H. Lu. 2003. MDM2 promotes p21waf1/cip1 proteasomal turnover independently of ubiquitylation. EMBO J. 22:6365-6377.
26. Jin, Y., S. X. Zeng, M. S. Dai, X. J. Yang, and H. Lu. 2002. MDM2 inhibits PCAF (p300/CREB-binding protein-associated factor)-mediated p53 acetylation. J. Biol. Chem. 277:30838-30843.
27. Jones, S. N., A. E. Roe, L. A. Donehower, and A. Bradley. 1995. Rescue of embryonic lethality in Mdm2-deficient mice by absence of p53. Nature 378:206-208.
28. Khanna, K. K., K. E. Keating, S. Kozlov, S. Scott, M. Gatei, K. Hobson, Y. Taya, B. Gabrielli, D. Chan, S. P. Lees-Miller, and M. F. Lavin. 1998. ATM associates with and phosphorylates p53: mapping the region of interaction. Nat. Genet. 20:398-400.
29. Kobet, E., X. Zeng, Y. Zhu, D. Keller, and H. Lu. 2000. MDM2 inhibits p300-mediated p53 acetytation and activation by forming a ternary complex with the two proteins. Proc. Natl. Acad. Sci. USA 97:12547-12552.
30. Kubbutat, M. H., S. N. Jones, and K. H. Vousden. 1997. Regulation of p53 stability by Mdm2. Nature 387:299-303.
31. Lane, D., and E. Harlow. 1982. Two different viral transforming proteins bind the same host tumour antigen. Nature 298:517.
32. Little, N. A., and A. G. Jochemsen. 2001. Hdmx and Mdm2 can repress transcription activation by p53 but not by p63. Oncogene 20:4576-4580.
33. Ljungman, M., F. Zhang, F. Chen, A. J. Rainbow, and B. C. McKay. 1999. Inhibition of RNA polymerase II as a trigger for the p53 response. Oncogene 18:583-592.
34. Lohrum, M. A., M. Ashcroft, M. H. Kubbutat, and K. H. Vousden. 2000. Contribution of two independent MDM2-binding domains in p14(ARF) to p53 stabilization. Curr. Biol. 10:539-542.
35. Lohrum, M. A., R. L. Ludwig, M. H. Kubbutat, M. Hanlon, and K. H. Vousden. 2003. Regulation of HDM2 activity by the ribosomal protein L11. Cancer Cell 3:577-587.
36. Lohrum, M. A., D. B. Woods, R. L. Ludwig, E. Balint, and K. H. Vousden. 2001. C-terminal ubiquitination of p53 contributes to nuclear export. Mol. Cell. Biol. 21:8521-8532.
37. Marechal, V., B. Elenbaas, J. Piette, J. C. Nicolas, and A. J. Levine. 1994. The ribosomal L5 protein is associated with mdm-2 and mdm-2-p53 complexes. Mol. Cell. Biol. 14:7414-7420.
38. Matsutake, T., and P. K. Srivastava. 2001. The immunoprotective MHC II epitope of a chemically induced tumor harbors a unique mutation in a ribosomal protein. Proc. Natl. Acad. Sci. USA 98:3992-3997.
39. Maya, R., M. Balass, S. T. Kim, D. Shkedy, J. F. Leal, O. Shifman, M. Moas, T. Buschmann, Z. Ronai, Y. Shiloh, M. B. Kastan, E. Katzir, and M. Oren. 2001. ATM-dependent phosphorylation of Mdm2 on serine 395: role in p53 activation by DNA damage. Genes Dev. 15:1067-1077.
40. Midgley, C. A., J. M. Desterro, M. K. Saville, S. Howard, A. Sparks, R. T. Hay, and D. P. Lane. 2000. An N-terminal p14ARF peptide blocks Mdm2-dependent ubiquitination in vitro and can activate p53 in vivo. Oncogene 19:2312-2323.
41. Momand, J., G. P. Zambetti, D. C. Olson, D. George, and A. J. Levine. 1992. The mdm-2 oncogene product forms a complex with the p53 protein and inhibits p53-mediated transactivation. Cell 69:1237-1245.
42. Monach, P. A., S. C. Meredith, C. T. Siegel, and H. Schreiber. 1995. A unique tumor antigen produced by a single amino acid substitution. Immunity 2:45-59.
43. Montes de Oca Luna, R., D. S. Wagner, and G. Lozano. 1995. Rescue of early embryonic lethality in mdm2-deficient mice by deletion of p53. Nature 378:203-206.
44. Naora, H. 1999. Involvement of ribosomal proteins in regulating cell growth and apoptosis: translational modulation or recruitment for extraribosomal activity? Immunol. Cell Biol. 77:197-205.
45. Neumann, F., and U. Krawinkel. 1997. Constitutive expression of human ribosomal protein L7 arrests the cell cycle in G1 and induces apoptosis in Jurkat T-lymphoma cells. Exp. Cell Res. 230:252-261.
46. Nikolaev, A. Y., M. Li, N. Puskas, J. Qin, and W. Gu. 2003. Parc: a cytoplasmic anchor for p53. Cell 112:29-40.
47. Oliner, J. D., J. A. Pietenpol, S. Thiagalingam, J. Gyuris, K. W. Kinzler, and B. Vogelstein. 1993. Oncoprotein MDM2 conceals the activation domain of tumour suppressor p53. Nature 362:857-860.
48. Oren, M., A. Damalas, T. Gottlieb, D. Michael, J. Taplick, J. F. Leal, R. Maya, M. Moas, R. Seger, Y. Taya, and A. Ben-Ze'Ev. 2002. Regulation of p53: intricate loops and delicate balances. Ann. N. Y. Acad. Sci. 973:374-383.
49. Palmero, I., C. Pantoja, and M. Serrano. 1998. p19ARF links the tumour suppressor p53 to Ras. Nature 395:125-126.
50. Pestov, D. G., Z. Strezoska, and L. F. Lau. 2001. Evidence of p53-dependent cross-talk between ribosome biogenesis and the cell cycle: effects of nucleolar protein Bop1 on G(1)/S transition. Mol. Cell. Biol. 21:4246-4255.
51. Picksley, S. M., and D. P. Lane. 1993. The p53-mdm2 autoregulatory feedback loop: a paradigm for the regulation of growth control by p53? Bioessays 15:689-690.
52. Ruggero, D., S. Grisendi, F. Piazza, E. Rego, F. Mari, P. H. Rao, C. Cordon-Cardo, and P. P. Pandolfi. 2003. Dyskeratosis congenita and cancer in mice deficient in ribosomal RNA modification. Science 299:259-262.
53. Ruggero, D., and P. P. Pandolfi. 2003. Does the ribosome translate cancer? Nat. Rev. Cancer 3:179-192.
54. Sharpless, N. E., and R. A. DePinho. 2002. p53: good cop/bad cop. Cell 110:9-12.
55. Shvarts, A., W. T. Steegenga, N. Riteco, T. van Laar, P. Dekker, M. Bazuine, R. C. van Ham, W. van der Houven van Oordt, G. Hateboer, A. J. van der Eb, and A. G. Jochemsen. 1996. MDMX: a novel p53-binding protein with some functional properties of MDM2. EMBO J. 15:5349-5357.
56. Siliciano, J. D., C. E. Canman, Y. Taya, K. Sakaguchi, E. Appella, and M. B. Kastan. 1997. DNA damage induces phosphorylation of the amino terminus of p53. Genes Dev. 11:3471-3481.
57. Stad, R., N. A. Little, D. P. Xirodimas, R. Frenk, A. J. van der Eb, D. P. Lane, M. K. Saville, and A. G. Jochemsen. 2001. Mdmx stabilizes p53 and Mdm2 via two distinct mechanisms. EMBO Rep. 2:1029-1034.
58. Strezoska, Z., D. G. Pestov, and L. F. Lau. 2002. Functional inactivation of the mouse nucleolar protein Bop1 inhibits multiple steps in pre-rRNA processing and blocks cell cycle progression. J. Biol. Chem. 277:29617-29625.
59. Sugimoto, M., M. L. Kuo, M. F. Roussel, and C. J. Sherr. 2003. Nucleolar Arf tumor suppressor inhibits ribosomal RNA processing. Mol. Cell 11:415-424.
60. Tao, W., and A. J. Levine. 1999. Nucleocytoplasmic shuttling of oncoprotein Hdm2 is required for Hdm2-mediated degradation of p53. Proc. Natl. Acad. Sci. USA 96:3077-3080.
61. Tao, W., and A. J. Levine. 1999. P19(ARF) stabilizes p53 by blocking nucleocytoplasmic shuttling of Mdm2. Proc. Natl. Acad. Sci. USA 96:6937-6941.
62. Tsai, R. Y., and R. D. McKay. 2002. A nucleolar mechanism controlling cell proliferation in stem cells and cancer cells. Genes Dev. 16:2991-3003.
63. Vogelstein, B., D. Lane, and A. J. Levine. 2000. Surfing the p53 network. Nature 408:307-310.
64. Voit, R., K. Schafer, and I. Grummt. 1997. Mechanism of repression of RNA polymerase I transcription by the retinoblastoma protein. Mol. Cell. Biol. 17:4230-4237.
65. Weber, J. D., M. L. Kuo, B. Bothner, E. L. DiGiammarino, R. W. Kriwacki, M. F. Roussel, and C. J. Sherr. 2000. Cooperative signals governing ARF-mdm2 interaction and nucleolar localization of the complex. Mol. Cell. Biol. 20:2517-2528.
66. Weber, J. D., L. J. Taylor, M. F. Roussel, C. J. Sherr, and D. Bar-Sagi. 1999. Nucleolar Arf sequesters Mdm2 and activates p53. Nat. Cell Biol. 1:20-26.
67. Wu, X., J. H. Bayle, D. Olson, and A. J. Levine. 1993. The p53-mdm-2 autoregulatory feedback loop. Genes Dev. 7:1126-1132.
68. Xirodimas, D., M. K. Saville, C. Edling, D. P. Lane, and S. Lain. 2001. Different effects of p14ARF on the levels of ubiquitinated p53 and Mdm2 in vivo. Oncogene 20:4972-4983.
69. Zalfa, F., M. Giorgi, B. Primerano, A. More, A. Di Penta, S. Reis, B. Oostra, and C. Bagni. 2003. The fragile X syndrome protein FMRP associates with BC1 RNA and regulates the translation of specific mRNAs at synapses. Cell 112:317-327.
70. Zeng, S. X., M. S. Dai, D. M. Keller, and H. Lu. 2002. SSRP1 functions as a co-activator of the transcriptional activator p63. EMBO J. 21:5487-5497.
71. Zeng, X., H. Lee, Q. Zhang, and H. Lu. 2001. p300 does not require its acetylase activity to stimulate p73 function. J. Biol. Chem. 276:48-52.
72. Zeng, X., X. Li, A. Miller, Z. Yuan, W. Yuan, R. P. Kwok, R. Goodman, and H. Lu. 2000. The N-terminal domain of p73 interacts with the CH1 domain of p300/CREB binding protein and mediates transcriptional activation and apoptosis. Mol. Cell. Biol. 20:1299-1310.
73. Zhai, W., and L. Comai. 2000. Repression of RNA polymerase I transcription by the tumor suppressor p53. Mol. Cell. Biol. 20:5930-5938.
74. Zhang, Y., G. W. Wolf, K. Bhat, A. Jin, T. Allio, W. A. Burkhart, and Y. Xiong. 2003. Ribosomal protein L11 negatively regulates oncoprotein MDM2 and mediates a p53-dependent ribosomal-stress checkpoint pathway. Mol. Cell. Biol. 23:8902-8912.
75. Zhang, Y., and Y. Xiong. 1999. Mutations in human ARF exon 2 disrupt its nucleolar localization and impair its ability to block nuclear export of MDM2 and p53. Mol. Cell 3:579-591.
76. Zhou, B. P., Y. Liao, W. Sa, Y. Zou, B. Spohn, and M. C. Hung. 2001. HER-2/neu induces p53 ubiquitination via Akt-mediated MDM2 phosphorylation. Nat. Cell Biol. 3:973-982.
77. Zindy, F., C. M. Eischen, D. H. Randle, T. Kamijo, J. L. Cleveland, C. J. Sherr, and M. F. Roussel. 1998. Myc signaling via the ARF tumor suppressor regulates p53-dependent apoptosis and immortalization. Genes Dev. 12:2424-2433.