Ribosomal Proteins RPL37, RPS15 and RPS20 Regulate the Mdm2-p53-MdmX Network

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Daftuar, Lilyn ^a   Zhu, Yan ^a   Jacq, Xavier ^b   Prives, Carol ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b Hybrigenics SA   (France)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN MDM2; PROTEIN MDMX; PROTEIN P53; PROTEIN RPL37; PROTEIN RPS15; PROTEIN RPS20; RIBOSOME PROTEIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE ARREST; CELL DEATH; DOWN REGULATION; GENETIC REGULATION; HUMAN; HUMAN CELL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STABILITY; REGULATORY MECHANISM;

EID: 84880753919     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0068667     Document Type: Article

References (54)

1. Levine AJ, Oren M, (2009) The first 30 years of p53: growing ever more complex. Nat Rev Cancer 9: 749-758.
2. Vousden KH, Prives C, (2009) Blinded by the Light: The Growing Complexity of p53. Cell 137: 413-431.
3. Toledo F, Wahl GM, (2006) Regulating the p53 pathway: in vitro hypotheses, in vivo veritas. Nat Rev Cancer 6: 909-923.
4. Shvarts A, Steegenga WT, Riteco N, van Laar T, Dekker P, et al. (1996) MDMX: a novel p53-binding protein with some functional properties of MDM2. EMBO J 15: 5349-5357.
5. Gu J, Kawai H, Nie L, Kitao H, Wiederschain D, et al. (2002) Mutual dependence of MDM2 and MDMX in their functional inactivation of p53. J Biol Chem 277: 19251-19254.
6. Tollini LA, Zhang Y, (2012) p53 Regulation Goes Live-Mdm2 and MdmX Co-Star: Lessons Learned from Mouse Modeling. Genes Cancer 3: 219-225.
7. Kawai H, Wiederschain D, Kitao H, Stuart J, Tsai KK, et al. (2003) DNA damage-induced MDMX degradation is mediated by MDM2. J Biol Chem 278: 45946-45953.
8. Biderman L, Poyurovsky MV, Assia Y, Manley JL, Prives C, (2012) MdmX is required for p53 interaction with and full induction of the Mdm2 promoter after cellular stress. Mol Cell Biol 32: 1214-1225.
9. Kruse JP, Gu W, (2009) Modes of p53 regulation. Cell 137: 609-622.
10. Momand J, Jung D, Wilczynski S, Niland J, (1998) The MDM2 gene amplification database. Nucleic Acids Res 26: 3453-3459.
11. Derezini M, Montanaro L, Trere D, (2009) What the nucleolus says to a tumor pathologist. Histopathology 54: 753-762.
12. Marechal V, Elenbaas B, Piette J, Nicolas JC, Levine AJ, (1994) The ribosomal L5 protein is associated with mdm-2 and mdm-2-p53 complexes. Mol Cell Biol 14: 7414-7420.
13. Lohrum MA, Ludwig RL, Kubbutat MH, Hanlon M, Vousden KH, (2003) Regulation of HDM2 activity by the ribosomal protein L11. Cancer Cell 3: 577-587.
14. Zhang Y, Wolf GW, Bhat K, Jin A, Allio T, et al. (2003) Ribosomal Protein L11 Negatively Regulates Oncoprotein MDM2 and Mediates a p53-Dependent Ribosomal-Stress Checkpoint Pathway. Mol Cell Biol 23: 8902-8912.
15. Gilkes DM, Chen L, Chen J, (2006) MDMX regulation of p53 response to ribosomal stress. EMBO J 25: 5614-5625.
16. Dai MS, Lu H, (2004) Inhibition of MDM2-mediated p53 ubiquitination and degradation by ribosomal protein L5. J Biol Chem 279: 44475-44482.
17. Dai MS, Zeng SX, Jin Y, Sun XX, David L, et al. (2004) Ribosomal protein L23 activates p53 by inhibiting MDM2 function in response to ribosomal perturbation but not to translation inhibition. Mol Cell Biol 24: 7654-7668.
18. Jin A, Itahana K, O'Keefe K, Zhang Y, (2004) Inhibition of HDM2 and activation of p53 by ribosomal protein L23. Mol Cell Biol 24: 7669-7680.
19. Chen D, Zhang Z, Li M, Wang W, Li Y, et al. (2007) Ribosomal protein S7 as a novel modulator of p53-MDM2 interaction: binding to MDM2, stabilization of p53 protein, and activation of p53 function. Oncogene 26: 5029-5037.
20. Zhu Y, Poyurovsky MV, Li Y, Biderman L, Stahl J, et al. (2009) Ribosomal Protein S7 Is Both a Regulator and a Substrate of MDM2. Mol Cell 35: 316-326.
21. Zhou X, Hao Q, Liao J, Zhang Q, Lu H, (2013) Ribosomal protein S14 unties the MDM2-p53 loop upon ribosomal stress. Oncogene 32: 388-396.
22. Zhang X, Wang W, Wang H, Wang MH, Xu W, et al. (2013) Identification of ribosomal protein S25 (RPS25)-MDM2-p53 regulatory feedback loop. Oncogene 32: 2782-2791.
23. Xiong X, Zhao Y, He H, Sun Y, (2011) Ribosomal protein S27-like and S27 interplay with p53-MDM2 axis as a target, a substrate and a regulator. Oncogene 30: 1798-1811.
24. Sun XX, Devine T, Challagundla KB, Dai MS, (2011) Interplay between Ribosomal Protein S27a and MDM2 Protein in p53 Activation in Response to Ribosomal Stress. J Biol Chem 286: 22730-22741.
25. Bursac S, Brdovcak MC, Pfannkuchen M, Orsolic I, Golomb L, et al. (2012) Mutual protection of ribosomal proteins L5 and L11 from degradation is essential for p53 activation upon ribosomal biogenesis stress. Proc Natl Acad Sci U S A 109: 20467-20472.
26. Lindström MS, Jin A, Deisenroth C, White Wolf G, Zhang Y, (2007) Cancer-associated mutations in the MDM2 zinc finger domain disrupt ribosomal protein interaction and attenuate MDM2-induced p53 degradation. Mol Cell Biol 27: 1056-1068.
27. Macias E, Jin A, Deisenroth C, Bhat K, Mao H, et al. (2010) An ARF-independent c-Myc-activated tumor suppression pathway mediated by ribosomal protein-Mdm2 interaction. Cancer Cell 18: 231-243.
28. Takagi M, Absalon MJ, McLure KG, Kastan MB, (2005) Regulation of p53 translation and induction after DNA damage by ribosomal protein L26 and nucleolin. Cell 123: 49-63.
29. Chen D, Kastan MB, (2010) 5′-3′-UTR interactions regulate p53 mRNA translation and provide a target for modulating p53 induction after DNA damage. Genes Dev 24: 2146-2156.
30. Ofir-Rosenfeld Y, Boggs K, Michael D, Kastan MB, Oren M, (2008) Mdm2 regulates p53 mRNA translation through inhibitory interactions with ribosomal protein L26. Mol Cell 32: 180-189.
31. Zhang Y, Wang J, Yuan Y, Zhang W, Guan W, et al. (2010) Negative regulation of HDM2 to attenuate p53 degradation by ribosomal protein L26. Nucleic Acids Res 38: 6544-6554.
32. Yadavilli S, Mayo LD, Higgins M, Lain S, Hegde V, et al. (2009) Ribosomal protein S3: A multi-functional protein that interacts with both p53 and MDM2 through its KH domain. DNA Repair (Amst) 8: 1215-1224.
33. Bunz F, Dutriaux A, Lengauer C, Waldman T, Zhou S, et al. (1998) Requirement for p53 and p21 to sustain G2 arrest after DNA damage. Science 282: 1497-1501.
34. Hermeking H, (2007) p53 enters the microRNA world. Cancer Cell 12: 414-418.
35. Yamakuchi M, Ferlito M, Lowenstein CJ, (2008) miR-34a repression of SIRT1 regulates apoptosis. Proc Natl Acad Sci U S A 105: 13421-13426.
36. Bensaad K, Tsuruta A, Selak MA, Vidal MN, Nakano K, et al. (2006) TIGAR, a p53-inducible regulator of glycolysis and apoptosis. Cell 126: 107-120.
37. Wade M, Li YC, Wahl GM, (2013) MDM2, MDMX and p53 in oncogenesis and cancer therapy. Nat Rev Cancer 13: 83-96.
38. Okamoto K, Li H, Jensen MR, Zhang T, Taya Y, et al. (2002) Cyclin G recruits PP2A to dephosphorylate Mdm2. Mol Cell 9: 761-771.
39. Ohtsuka T, Jensen MR, Kim HG, Kim KT, Lee SW, (2004) The negative role of cyclin G in ATM-dependent p53 activation. Oncogene 23: 5405-5408.
40. Morgado-Palacin L, Llanos S, Serrano M, (2012) Ribosomal stress induces L11- and p53-dependent apoptosis in mouse pluripotent stem cells. Cell Cycle 11: 503-510.
41. Mahata B, Sundqvist A, Xirodimas DP, (2012) Recruitment of RPL11 at promoter sites of p53-regulated genes upon nucleolar stress through NEDD8 and in an Mdm2-dependent manner. Oncogene 31: 3060-3071.
42. Tanimura S, Ohtsuka S, Mitsui K, Shirouzu K, Yoshimura A, et al. (1999) MDM2 interacts with MDMX through their RING finger domains. FEBS Lett 447: 5-9.
43. Linke K, Mace PD, Smith CA, Vaux DL, Silke J, et al. (2008) Structure of the MDM2/MDMX RING domain heterodimer reveals dimerization is required for their ubiquitylation in trans. Cell Death Differ 15: 841-848.
44. Llanos S, Serrano M, (2010) Depletion of ribosomal protein L37 occurs in response to DNA damage and activates p53 through the L11/MDM2 pathway. Cell Cycle 9: 4005-4012.
45. Gazda HT, Sheen MR, Vlachos A, Choesmel V, O'Donohue MF, et al. (2008) Ribosomal protein L5 and L11 mutations are associated with cleft palate and abnormal thumbs in Diamond-Blackfan anemia patients. Am J Hum Genet 83: 769-780.
46. Amsterdam A, Sadler KC, Lai K, Farrington S, Bronson RT, et al. (2004) Many ribosomal protein genes are cancer genes in zebrafish. PLoS Biol 2: E139.
47. McGowan KA, Li JZ, Park CY, Beaudry V, Tabor HK, et al. (2008) Ribosomal mutations cause p53-mediated dark skin and pleiotropic effects. Nat Genet 40: 963-970.
48. Fumagalli S, Di Cara A, Neb-Gulati A, Natt F, Schwemberger S, et al. (2009) Absence of nucleolar disruption after impairment of 40S ribosome biogenesis reveals an rpL11-translation-dependent mechanism of p53 induction. Nat Cell Biol 11: 501-508.
49. Sun XX, Wang YG, Xirodimas DP, Dai MS, (2010) Perturbation of 60 S ribosomal biogenesis results in ribosomal protein L5- and L11-dependent p53 activation. J Biol Chem 285: 25812-25821.
50. Fumagalli S, Ivanenkov VV, Teng T, Thomas G, (2012) Suprainduction of p53 by disruption of 40S and 60S ribosome biogenesis leads to the activation of a novel G2/M checkpoint. Genes Dev 26: 1028-1040.
51. Daftuar L, Zhu Y, Prives C, (2010) Ribosomal protein L37 and the p53 network. Cell Cycle 9: 4259.
52. Barkić M, Crnomarković S, Grabusić K, Bogetić I, Panić L, et al. (2009) The p53 tumor suppressor causes congenital malformations in Rpl24-deficient mice and promotes their survival. Mol Cell Biol 29: 2489-2504.
53. Lindström MS, Nistér M, (2010) Silencing of ribosomal protein S9 elicits a multitude of cellular responses inhibiting the growth of cancer cells subsequent to p53 activation. PLoS One 5: e9578.
54. Peart MJ, Poyurovsky MV, Kass EM, Urist M, Verschuren EW, et al. (2010) APC/C(Cdc20) targets E2F1 for degradation in prometaphase. Cell Cycle 9: 3956-3964.