Ubiquitin and ubiquitin-like proteins in the nucleolus: Multitasking tools for a ribosome factory

Genes and Cancer

Volumn 1, Issue 7, 2010, Pages 681-689

  Shcherbik, Natalia ^a   Pestov, Dimitri G ^a  

^a UNIVERSITY OF MEDICINE AND DENTISTRY OF NEW JERSEY   (United States)

Author keywords

Mdm2; Nucleolar stress; p53; Ribosomal proteins; Ribosome biogenesis; Ubiquitin

Indexed keywords

ARF PROTEIN; FIBRILLARIN; NUCLEOPHOSMIN; PROTEASOME; PROTEIN MDM2; PROTEIN P14; PROTEIN P53; RIBOSOME RNA; SUMO PROTEIN; UBIQUITIN; UBIQUITIN PROTEIN LIGASE E3; UBIQUITINATED PROTEIN;

APOPTOSIS; ARTICLE; BIOGENESIS; CARCINOGENICITY; CELL CYCLE ARREST; CELL CYCLE PROGRESSION; CELL GROWTH; CELL PROLIFERATION; CELL STRESS; CYTOPLASM; DNA REPAIR; ENZYME ACTIVITY; FRAMESHIFT MUTATION; HUMAN; NONHUMAN; NONSENSE MUTATION; NUCLEOLUS; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; RIBOSOME; SUMOYLATION; UBIQUITINATION; UPREGULATION;

MAMMALIA;

EID: 79952858979     PISSN: 19476019     EISSN: 19476027     Source Type: Journal    
DOI: 10.1177/1947601910381382     Document Type: Article

References (123)

1. Kerscher O, Felberbaum R, Hochstrasser M. Modification of proteins by ubiquitin and ubiquitin like proteins. Annu Rev Cell Dev Biol.2006;22:159-80.
2. Mayer C, Grummt I. Ribosome biogenesis and cell growth: mTOR coordinates transcription by all three classes of nuclear RNA polymerases. Oncogene. 2006;25:6384-91.
3. Lempiäinen H, Shore D. Growth control and ribosome biogenesis. Curr Opin Cell Biol.2009;21:855-63.
4. Kressler D, Hurt E, Baßler J. Driving ribosome assembly. Biochim Biophys Acta.2010;1803:673-83.
5. Raska I, Shaw PJ, Cmarko D. New insights into nucleolar architecture and activity. Int Rev Cytol.2006;255:177-235.
6. Sirri V, Urcuqui-Inchima S, Roussel P, Hernandez- Verdun D. Nucleolus: the fascinating nuclear body. Histochem Cell Biol. 2008;129:13-31.
7. Boisvert F, van Koningsbruggen S, Navascués J, Lamond AI. The multifunctional nucleolus. Nat Rev Mol Cell Biol. 2007;8:574-85.
8. Derenzini M, Trerè D, Pession A, Montanaro L, Sirri V, Ochs RL. Nucleolar function and size in cancer cells. Am J Pathol. 1998;152:1291-7.
9. Ruggero D, Pandolfi PP. Does the ribosome translate cancer? Nat Rev Cancer. 2003;3:179-92.
10. Montanaro L, Treré D, Derenzini M. Nucleolus, ribosomes, and cancer. Am J Pathol.2008;173:301-10.
11. Lewis JD, Tollervey D. Like attracts like: getting RNA processing together in the nucleus. Science.2000;288:1385-9.
12. Meyuhas O. Synthesis of the translational apparatus is regulated at the translational level. Eur J Biochem. 2000;267:6321-30.
13. Warner JR. In the absence of ribosomal RNA synthesis, the ribosomal proteins of HeLa cells are synthesized normally and degraded rapidly. J Mol Biol. 1977;115:315-33.
14. Lam YW, Lamond AI, Mann M, Andersen JS. Analysis of nucleolar protein dynamics reveals the nuclear degradation of ribosomal proteins. Curr Biol. 2007;17:749-60.
15. Andersen JS, Lam YW, Leung AKL, et al. Nucleolar proteome dynamics. Nature. 2005; 433:77-83.
16. Wójcik C, DeMartino GN. Intracellular localization of proteasomes. Int J Biochem Cell Biol.2003;35:579-89.
17. Rockel TD, Stuhlmann D, von Mikecz A. Proteasomes degrade proteins in focal subdomains of the human cell nucleus. J Cell Sci.2005;118:5231-42.
18. Arabi A, Rustum C, Hallberg E, Wright APH. Accumulation of c-Myc and proteasomes at the nucleoli of cells containing elevated c-Myc protein levels. J Cell Sci. 2003;116:1707-17.
19. Scharf A, Rockel TD, von Mikecz A. Localization of proteasomes and proteasomal proteolysis in the mammalian interphase cell nucleus by systematic application of immunocytochemistry. Histochem Cell Biol. 2007;127:591-601.
20. Peng J, Schwartz D, Elias JE, et al. A proteomics approach to understanding protein ubiquitination. Nat Biotechnol. 2003;21:921-6.
21. Matsumoto M, Hatakeyama S, Oyamada K, Oda Y, Nishimura T, Nakayama KI. Large-scale analysis of the human ubiquitin-related proteome. Proteomics. 2005;5:4145-51.
22. Xirodimas DP, Sundqvist A, Nakamura A, Shen L, Botting C, Hay RT. Ribosomal proteins are targets for the NEDD8 pathway. EMBO Rep.2008;9:280-6.
23. Matafora V, D'Amato A, Mori S, Blasi F, Bachi A. Proteomics analysis of nucleolar SUMO-1 target proteins upon proteasome inhibition. Mol Cell Proteomics. 2009;8:2243-55.
24. Finley D, Bartel B, Varshavsky A. The tails of ubiquitin precursors are ribosomal proteins whose fusion to ubiquitin facilitates ribosome biogenesis. Nature. 1989;338:394-401.
25. Redman KL, Rechsteiner M. Identification of the long ubiquitin extension as ribosomal protein S27a. Nature. 1989;338:438-40.
26. Chan YL, Suzuki K, Wool IG. The carboxyl extensions of two rat ubiquitin fusion proteins are ribosomal proteins S27a and L40. Biochem Biophys Res Commun. 1995;215:682-90.
27. Finley D, Ozkaynak E, Varshavsky A. The yeast polyubiquitin gene is essential for resistance to high temperatures, starvation, and other stresses. Cell. 1987;48:1035-46.
28. Catic A, Sun ZJ, Ratner DM, et al. Sequence and structure evolved separately in a ribosomal ubiquitin variant. EMBO J. 2007;26:3474-83.
29. Olvera J, Wool IG. The carboxyl extension of a ubiquitin-like protein is rat ribosomal protein S30. J Biol Chem. 1993;268:17967-74.
30. Lacombe T, García-Gómez JJ, de la Cruz J, et al. Linear ubiquitin fusion to Rps31 and its subsequent cleavage are required for the efficient production and functional integrity of 40S ribosomal subunits. Mol Microbiol. 2009;72:69-84.
31. Stavreva DA, Kawasaki M, Dundr M, et al. Potential roles for ubiquitin and the proteasome during ribosome biogenesis. Mol Cell Biol.2006;26:5131-45.
32. Fátyol K, Grummt I. Proteasomal ATPases are associated with rDNA: the ubiquitin proteasome system plays a direct role in RNA polymerase I transcription. Biochim Biophys Acta.2008;1779:850-9.
33. Chen M, Rockel T, Steinweger G, Hemmerich P, Risch J, von Mikecz A. Subcellular recruitment of fibrillarin to nucleoplasmic proteasomes: implications for processing of a nucleolar autoantigen. Mol Biol Cell. 2002;13:3576-87.
34. Sharma P, Murillas R, Zhang H, Kuehn MR. N4BP1 is a newly identified nucleolar protein that undergoes SUMO-regulated polyubiquitylation and proteasomal turnover at promyelocytic leukemia nuclear bodies. J Cell Sci. 2010;123:1227-34.
35. Endo A, Matsumoto M, Inada T, et al. Nucleolar structure and function are regulated by the deubiquitylating enzyme USP36. J Cell Sci.2009;122:678-86.
36. LaRiviere FJ, Cole SE, Ferullo DJ, Moore MJ. A late-acting quality control process for mature eukaryotic rRNAs. Mol Cell. 2006;24:619-26.
37. Fujii K, Kitabatake M, Sakata T, Miyata A, Ohno M. A role for ubiquitin in the clearance of nonfunctional rRNAs. Genes Dev. 2009;23:963-74.
38. Hochstrasser M. Origin and function of ubiquitinlike proteins. Nature. 2009;458:422-9.
39. Sundqvist A, Liu G, Mirsaliotis A, Xirodimas DP. Regulation of nucleolar signalling to p53 through NEDDylation of L11. EMBO Rep. 2009;10:1132-9.
40. Panse VG, Kressler D, Pauli A, et al. Formation and nuclear export of preribosomes are functionally linked to the small-ubiquitin-related modifier pathway. Traffic. 2006;7:1311-21.
41. Nishida T, Tanaka H, Yasuda H. A novel mammalian Smt3-specific isopeptidase 1 (SMT3IP1) localized in the nucleolus at interphase. Eur J Biochem. 2000;267:6423-7.
42. Di Bacco A, Ouyang J, Lee H, Catic A, Ploegh H, Gill G. The SUMO-specific protease SENP5 is required for cell division. Mol Cell Biol.2006;26:4489-98.
43. Gong L, Yeh ETH. Characterization of a family of nucleolar SUMO-specific proteases with preference for SUMO-2 or SUMO-3. J Biol Chem.2006;281:15869-77.
44. Yun C, Wang Y, Mukhopadhyay D, et al. Nucleolar protein B23/nucleophosmin regulates the vertebrate SUMO pathway through SENP3 and SENP5 proteases. J Cell Biol. 2008;183:589-95.
45. Haindl M, Harasim T, Eick D, Muller S. The nucleolar SUMO-specific protease SENP3 reverses SUMO modification of nucleophosmin and is required for rRNA processing. EMBO Rep. 2008;9:273-9.
46. Nacerddine K, Lehembre F, Bhaumik M, et al. The SUMO pathway is essential for nuclear integrity and chromosome segregation in mice. Dev Cell. 2005;9:769-79.
47. Visintin R, Amon A. The nucleolus: the magician's hat for cell cycle tricks. Curr Opin Cell Biol. 2000;12:372-7.
48. Zunino R, Braschi E, Xu L, McBride HM. Translocation of SenP5 from the nucleoli to the mitochondria modulates DRP1-dependent fission during mitosis. J Biol Chem. 2009;284:17783-95.
49. Volarevic S, Stewart MJ, Ledermann B, et al. Proliferation, but not growth, blocked by conditional deletion of 40S ribosomal protein S6. Science.2000;288:2045-7.
50. Pestov DG, Strezoska Z, Lau LF. 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.2001;21:4246-55.
51. Yuan X, Zhou Y, Casanova E, et al. 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.
52. Rubbi CP, Milner J. Disruption of the nucleolus mediates stabilization of p53 in response to DNA damage and other stresses. EMBO J.2003;22:6068-77.
53. Burger K, Mühl B, Harasim T, et al. Chemotherapeutic drugs inhibit ribosome biogenesis at various levels. J Biol Chem. 2010;285:12416-25.
54. Hölzel M, Rohrmoser M, Schlee M, et al. Mammalian WDR12 is a novel member of the Pes1- Bop1 complex and is required for ribosome biogenesis and cell proliferation. J Cell Biol.2005;170:367-78.
55. Fumagalli S, Di Cara A, Neb-Gulati A, et al. Absence of nucleolar disruption after impairment of 40S ribosome biogenesis reveals an rpL11- translation-dependent mechanism of p53 induction. Nat Cell Biol. 2009;11:501-8.
56. Hölzel M, Orban M, Hochstatter J, et al. Defects in 18 S or 28 S rRNA processing activate the p53 pathway. J Biol Chem. 2010;285:6364-70.
57. Lindström MS, Nistér 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.
58. Horn HF, Vousden KH. Coping with stress: multiple ways to activate p53. Oncogene.2007;26:1306-16.
59. Murray-Zmijewski F, Slee EA, Lu X. A complex barcode underlies the heterogeneous response of p53 to stress. Nat Rev Mol Cell Biol. 2008;9: 702-12.
60. Panic L, Tamarut S, Sticker-Jantscheff M, et al. Ribosomal protein S6 gene haploinsufficiency is associated with activation of a p53-dependent checkpoint during gastrulation. Mol Cell Biol.2006;26:8880-91.
61. Azuma M, Toyama R, Laver E, Dawid IB. Perturbation of rRNA synthesis in the bap28 mutation leads to apoptosis mediated by p53 in the zebrafish central nervous system. J Biol Chem.2006;281:13309-16.
62. Chakraborty A, Uechi T, Higa S, Torihara H, Kenmochi N. Loss of ribosomal protein L11 affects zebrafish embryonic development through a p53-dependent apoptotic response. PLoS One.2009;4:e4152.
63. Zhang Y, Lu H. Signaling to p53: ribosomal proteins find their way. Cancer Cell. 2009;16:369-77.
64. Warner JR, McIntosh KB. How common are extraribosomal functions of ribosomal proteins? Mol Cell. 2009;34:3-11.
65. Brooks CL, Gu W. p53 ubiquitination: Mdm2 and beyond. Mol Cell. 2006;21:307-15.
66. Coutts AS, Adams CJ, La Thangue NB. p53 ubiquitination by Mdm2: a never ending tail? DNA Repair (Amst). 2009;8:483-90.
67. Honda R, Tanaka H, Yasuda H. Oncoprotein MDM2 is a ubiquitin ligase E3 for tumor suppressor p53. FEBS Lett. 1997;420:25-7.
68. Fang S, Jensen JP, Ludwig RL, Vousden KH, Weissman AM. Mdm2 is a RING finger-dependent ubiquitin protein ligase for itself and p53. J Biol Chem. 2000;275:8945-51.
69. Wu X, Bayle JH, Olson D, Levine AJ. The p53- mdm-2 autoregulatory feedback loop. Genes Dev. 1993;7:1126-32.
70. Harris SL, Levine AJ. The p53 pathway: positive and negative feedback loops. Oncogene.2005;24:2899-908.
71. Montes de Oca Luna R, Wagner DS, Lozano G. Rescue of early embryonic lethality in mdm2-deficient mice by deletion of p53. Nature. 1995;378:203-6.
72. Jones SN, Roe AE, Donehower LA, Bradley A. Rescue of embryonic lethality in Mdm2-deficient mice by absence of p53. Nature. 1995;378:206-8.
73. Marechal V, Elenbaas B, Piette J, Nicolas JC, Levine AJ. The ribosomal L5 protein is associated with mdm-2 and mdm-2-p53 complexes. Mol Cell Biol. 1994;14:7414-20.
74. Lohrum MAE, Ludwig RL, Kubbutat MHG, Hanlon M, Vousden KH. Regulation of HDM2 activity by the ribosomal protein L11. Cancer Cell. 2003;3:577-87.
75. Zhang Y, Wolf GW, Bhat K, et al. Ribosomal protein L11 negatively regulates oncoprotein MDM2 and mediates a p53-dependent ribosomalstress checkpoint pathway. Mol Cell Biol. 2003;23: 8902-12.
76. Bhat KP, Itahana K, Jin A, Zhang Y. Essential role of ribosomal protein L11 in mediating growth inhibition-induced p53 activation. EMBO J. 2004;23:2402-12.
77. Dai M, Zeng SX, Jin Y, Sun 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;24:7654-68.
78. Dai M, Lu H. Inhibition of MDM2-mediated p53 ubiquitination and degradation by ribosomal protein L5. J Biol Chem. 2004;279:44475-82.
79. Jin A, Itahana K, O'Keefe K, Zhang Y. Inhibition of HDM2 and activation of p53 by ribosomal protein L23. Mol Cell Biol. 2004;24:7669-80.
80. Lindström MS, Jin A, Deisenroth C, White Wolf G, Zhang Y. Cancer-associated mutations in the MDM2 zinc finger domain disrupt ribosomal protein interaction and attenuate MDM2-induced p53 degradation. Mol Cell Biol. 2007;27:1056-68.
81. Chen D, Zhang Z, Li M, et al. Ribosomal protein S7 as a novel modulator of p53-MDM2 interaction: binding to MDM2, stabilization of p53 protein, and activation of p53 function. Oncogene.2007;26:5029-37.
82. Zhu Y, Poyurovsky MV, Li Y, et al. Ribosomal protein S7 is both a regulator and a substrate of MDM2. Mol Cell. 2009;35:316-26.
83. Yadavilli S, Mayo LD, Higgins M, Lain S, Hegde V, Deutsch WA. Ribosomal protein S3: a multifunctional protein that interacts with both p53 and MDM2 through its KH domain. DNA Repair (Amst). 2009;8:1215-24.
84. Sun X, Dai M, Lu H. 5-fluorouracil activation of p53 involves an MDM2-ribosomal protein interaction. J Biol Chem. 2007;282:8052-9.
85. Sun X, Dai M, Lu H. Mycophenolic acid activation of p53 requires ribosomal proteins L5 and L11. J Biol Chem. 2008;283:12387-92.
86. Gilkes DM, Chen L, Chen J. MDMX regulation of p53 response to ribosomal stress. EMBO J.2006;25:5614-25.
87. Horn HF, Vousden KH. Cooperation between the ribosomal proteins L5 and L11 in the p53 pathway. Oncogene. 2008;27:5774-84.
88. Schlott T, Reimer S, Jahns A, et al. Point mutations and nucleotide insertions in the MDM2 zinc finger structure of human tumours. J Pathol.1997;182:54-61.
89. Linares LK, Hengstermann A, Ciechanover A, Müller S, Scheffner M. HdmX stimulates Hdm2- mediated ubiquitination and degradation of p53. Proc Natl Acad Sci U S A. 2003;100:12009-14.
90. Wade M, Wang YV, Wahl GM. The p53 orchestra: Mdm2 and Mdmx set the tone. Trends Cell Biol. 2010;20:299-309.
91. Sherr CJ. Divorcing ARF and p53: an unsettled case. Nat Rev Cancer. 2006;6:663-73.
92. Weber JD, Taylor LJ, Roussel MF, Sherr CJ, Bar-Sagi D. Nucleolar Arf sequesters Mdm2 and activates p53. Nat Cell Biol. 1999;1:20-6.
93. Llanos S, Clark PA, Rowe J, Peters G. Stabilization of p53 by p14ARF without relocation of MDM2 to the nucleolus. Nat Cell Biol. 2001;3:445-52.
94. Korgaonkar C, Zhao L, Modestou M, Quelle DE. ARF function does not require p53 stabilization or Mdm2 relocalization. Mol Cell Biol.2002;22:196-206.
95. Kuo M, den Besten W, Thomas MC, Sherr CJ. Arf-induced turnover of the nucleolar nucleophosmin- associated SUMO-2/3 protease Senp3. Cell Cycle. 2008;7:3378-87.
96. Bertwistle D, Sugimoto M, Sherr CJ. Physical and functional interactions of the Arf tumor suppressor protein with nucleophosmin/B23. Mol Cell Biol. 2004;24:985-96.
97. Rizos H, McKenzie HA, Ayub AL, et al. Physical and functional interaction of the p14ARF tumor suppressor with ribosomes. J Biol Chem.2006;281:38080-8.
98. Sugimoto M, Kuo M, Roussel MF, Sherr CJ. Nucleolar Arf tumor suppressor inhibits ribosomal RNA processing. Mol Cell. 2003;11: 415-24.
99. Itahana K, Bhat KP, Jin A, et al. Tumor suppressor ARF degrades B23, a nucleolar protein involved in ribosome biogenesis and cell proliferation. Mol Cell. 2003;12:1151-64.
100. Grisendi S, Bernardi R, Rossi M, et al. Role of nucleophosmin in embryonic development and tumorigenesis. Nature. 2005;437:147-53.
101. Borer RA, Lehner CF, Eppenberger HM, Nigg EA. Major nucleolar proteins shuttle between nucleus and cytoplasm. Cell. 1989;56:379-90.
102. Lindström MS, Zhang Y. Ribosomal protein S9 is a novel B23/NPM-binding protein required for normal cell proliferation. J Biol Chem. 2008;283: 15568-76.
103. Maggi LBJ, Kuchenruether M, Dadey DYA, et al. Nucleophosmin serves as a rate-limiting nuclear export chaperone for the Mammalian ribosome. Mol Cell Biol. 2008;28:7050-65.
104. Korgaonkar C, Hagen J, Tompkins V, et al. Nucleophosmin (B23) targets ARF to nucleoli and inhibits its function. Mol Cell Biol. 2005;25:1258-71.
105. Kuo M, den Besten W, Bertwistle D, Roussel MF, Sherr CJ. N-terminal polyubiquitination and degradation of the Arf tumor suppressor. Genes Dev.2004;18:1862-74.
106. Brady SN, Yu Y, Maggi LBJ, Weber JD. ARF impedes NPM/B23 shuttling in an Mdm2- sensitive tumor suppressor pathway. Mol Cell Biol. 2004;24:9327-38.
107. Wang YV, Wade M, Wong E, Li Y, Rodewald LW, Wahl GM. Quantitative analyses reveal the importance of regulated Hdmx degradation for p53 activation. Proc Natl Acad Sci U S A.2007;104:12365-70.
108. Freedman DA, Levine AJ. Nuclear export is required for degradation of endogenous p53 by MDM2 and human papillomavirus E6. Mol Cell Biol. 1998;18:7288-93.
109. Tao W, Levine AJ. Nucleocytoplasmic shuttling of oncoprotein Hdm2 is required for Hdm2- mediated degradation of p53. Proc Natl Acad Sci U S A. 1999;96:3077-80.
110. O'Keefe K, Li H, Zhang Y. Nucleocytoplasmic shuttling of p53 is essential for MDM2-mediated cytoplasmic degradation but not ubiquitination. Mol Cell Biol. 2003;23:6396-405.
111. Erster S, Mihara M, Kim RH, Petrenko O, Moll UM. In vivo mitochondrial p53 translocation triggers a rapid first wave of cell death in response to DNA damage that can precede p53 target gene activation. Mol Cell Biol. 2004;24: 6728-41.
112. Marchenko ND, Wolff S, Erster S, Becker K, Moll UM. Monoubiquitylation promotes mitochondrial p53 translocation. EMBO J. 2007;26:923-34.
113. Tasdemir E, Maiuri MC, Galluzzi L, et al. Regulation of autophagy by cytoplasmic p53. Nat Cell Biol. 2008;10:676-87.
114. Boyd SD, Tsai KY, Jacks T. An intact HDM2 RING-finger domain is required for nuclear exclusion of p53. Nat Cell Biol. 2000;2:563-8.
115. Geyer RK, Yu ZK, Maki CG. The MDM2 RINGfinger domain is required to promote p53 nuclear export. Nat Cell Biol. 2000;2:569-73.
116. Lohrum MA, Woods DB, Ludwig RL, Bálint E, Vousden KH. C-terminal ubiquitination of p53 contributes to nuclear export. Mol Cell Biol.2001;21:8521-32.
117. Takagi M, Absalon MJ, McLure KG, Kastan MB. Regulation of p53 translation and induction after DNA damage by ribosomal protein L26 and nucleolin. Cell. 2005;123:49-63.
118. Ofir-Rosenfeld Y, Boggs K, Michael D, Kastan MB, Oren M. Mdm2 regulates p53 mRNA translation through inhibitory interactions with ribosomal protein L26. Mol Cell. 2008;32:180-9.
119. Dornan D, Wertz I, Shimizu H, et al. The ubiquitin ligase COP1 is a critical negative regulator of p53. Nature. 2004;429:86-92.
120. Leng RP, Lin Y, Ma W, et al. Pirh2, a p53-induced ubiquitin-protein ligase, promotes p53 degradation. Cell. 2003;112:779-91.
121. Chen D, Kon N, Li M, Zhang W, Qin J, Gu W. ARF-BP1/Mule is a critical mediator of the ARF tumor suppressor. Cell. 2005;121:1071-83.
122. Le Cam L, Linares LK, Paul C, et al. E4F1 is an atypical ubiquitin ligase that modulates p53 effector functions independently of degradation. Cell.2006;127:775-88.
123. Narla A, Ebert BL. Ribosomopathies: human disorders of ribosome dysfunction. Blood.2010;115:3196-205.