Ribosomal stress induces L11- and p53-dependent apoptosis in mouse pluripotent stem cells

Cell Cycle

Volumn 11, Issue 3, 2012, Pages 503-510

  Morgado Palacin, Lucia ^a   Llanos, Susana ^a   Serrano, Manuel ^a  

^a Centro Nacional de Investigaciones Oncológicas   (Spain)

Author keywords

Apoptosis; Embryonic stem cells; Induced pluripotent stem cells; p53; Ribosomal stress

Indexed keywords

CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37; DACTINOMYCIN; PROTEIN BAX; PROTEIN MDM2; PROTEIN NOXA; PROTEIN P21; PROTEIN P53; PUMA PROTEIN; RIBOSOMAL PROTEIN L1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL CYCLE CHECKPOINT; CELL STRESS; CONTROLLED STUDY; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; LOW DRUG DOSE; MOUSE; NONHUMAN; PLURIPOTENT STEM CELL; PROTEIN DEPLETION; RIBOSOME; TRANSCRIPTION REGULATION;

EID: 84857198383     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.11.3.19002     Document Type: Article

References (33)

1. Junttila MR, Evan GI. p53 - a Jack of all trades but master of none. Nat Rev Cancer 2009; 9:821-9; PMID:19776747; http://dx.doi.org/10.1038/nrc2728.
2. Meek DW. Tumour suppression by p53: a role for the DNA damage response? Nat Rev Cancer 2009; 9:714-23; PMID:19730431.
3. Kruse JP, Gu W. Modes of p53 regulation. Cell 2009; 137:609-22; PMID:19450511; http://dx.doi.org/10.1016/j.cell.2009.04.050.
4. Marine JC, Lozano G. Mdm2-mediated ubiquitylation: p53 and beyond. Cell Death Differ 2010; 17:93-102; PMID:19498444; http://dx.doi.org/10.1038/cdd.2009. 68.
5. Zhang Y, Lu H. Signaling to p53: ribosomal proteins find their way. Cancer Cell 2009; 16:369-77; PMID:19878869; http://dx.doi.org/10.1016/j.ccr. 2009.09.024.
6. Deisenroth C, Zhang Y. Ribosome biogenesis surveillance: probing the ribosomal protein-Mdm2-p53 pathway. Oncogene 2010; 29:4253-60; PMID:20498634; http://dx.doi.org/10.1038/onc.2010.189.
7. Lohrum MA, Ludwig RL, Kubbutat MH, Hanlon M, Vousden KH. Regulation of HDM2 activity by the ribosomal protein L11. Cancer Cell 2003; 3:577-87; PMID:12842086; http://dx.doi.org/10.1016/S1535-6108(03)00134-X.
8. Zhang Y, Wolf GW, Bhat K, Jin A, Allio T, Burkhart WA, et al. Ribosomal protein L11 negatively regulates oncoprotein MDM2 and mediates a p53-dependent ribosomal-stress checkpoint pathway. Mol Cell Biol 2003; 23:8902-12; PMID:14612427; http://dx.doi.org/10.1128/MCB.23.23.8902-8912.2003.
9. Fumagalli S, Di Cara A, Neb-Gulati A, Natt F, Schwemberger S, Hall J, 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; PMID:19287375; http://dx.doi.org/10.1038/ncb1858.
10. Macias E, Jin A, Deisenroth C, Bhat K, Mao H, Lindström MS, et al. An ARF-independent c-MYC-activated tumor suppression pathway mediated by ribosomal protein-Mdm2 Interaction. Cancer Cell 2010; 18:231-43; PMID:20832751; http://dx.doi.org/10.1016/j.ccr.2010.08.007.
11. Dai MS, Lu H. Inhibition of MDM2-mediated p53 ubiquitination and degradation by ribosomal protein L5. J Biol Chem 2004; 279:44475-82; PMID:15308643; http://dx.doi.org/10.1074/jbc.M403722200.
12. 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; PMID:15314174; http://dx.doi.org/10.1128/MCB.24.17.7669-7680.2004.
13. Chen D, Zhang Z, Li M, Wang W, Li Y, Rayburn ER, 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; PMID:17310983; http://dx.doi.org/10.1038/sj.onc.1210327.
14. Zhu Y, Poyurovsky MV, Li Y, Biderman L, Stahl J, Jacq X, et al. Ribosomal protein S7 is both a regulator and a substrate of MDM2. Mol Cell 2009; 35:316-26; PMID:19683495; http://dx.doi.org/10.1016/j.molcel.2009.07.014.
15. Narla A, Ebert BL. Ribosomopathies: human disorders of ribosome dysfunction. Blood 2010; 115:3196-205; PMID:20194897; http://dx.doi.org/10.1182/ blood-2009-10-178129.
16. Caldarola S, De Stefano MC, Amaldi F, Loreni F. Synthesis and function of ribosomal proteins - fading models and new perspectives. FEBS J 2009; 276:3199-210; PMID:19438715; http://dx.doi.org/10.1111/j.1742-4658.2009.07036.x.
17. Llanos S, Serrano M. Depletion of ribosomal protein L37 occurs in response to DNA damage and activates p53 through the L11/MDM2 pathway. Cell Cycle 2010; 9:4005-12; PMID:20935493; http://dx.doi.org/10.4161/cc.9.19.13299.
18. White J, Dalton S. Cell cycle control of embryonic stem cells. Stem Cell Rev 2005; 1:131-8; PMID:17142847; http://dx.doi.org/10.1385/SCR:1:2:131.
19. Ballabeni A, Park IH, Zhao R, Wang W, Lerou PH, Daley GQ, et al. Cell cycle adaptations of embryonic stem cells. Proc Natl Acad Sci USA 2011; 108:19252-7; PMID:22084091; http://dx.doi.org/10.1073/pnas.1116794108.
20. Sabapathy K, Klemm M, Jaenisch R, Wagner EF. Regulation of ES cell differentiation by functional and conformational modulation of p53. EMBO J 1997; 16:6217-29; PMID:9321401; http://dx.doi.org/10.1093/emboj/16.20.6217.
21. Corbet SW, Clarke AR, Gledhill S, Wyllie AH. P53-dependent and -independent links between DNAdamage, apoptosis and mutation frequency in ES cells. Oncogene 1999; 18:1537-44; PMID:10102623; http://dx.doi.org/10.1038/sj. onc.1202436.
22. Chao C, Saito S, Kang J, Anderson CW, Appella E, Xu Y. p53 transcriptional activity is essential for p53-dependent apoptosis following DNA damage. EMBO J 2000; 19:4967-75; PMID:10990460; http://dx.doi.org/10.1093/emboj/ 19.18.4967.
23. Han MK, Song EK, Guo Y, Ou X, Mantel C, Broxmeyer HE. SIRT1 regulates apoptosis and Nanog expression in mouse embryonic stem cells by controlling p53 subcellular localization. Cell Stem Cell 2008; 2:241-51; PMID:18371449; http://dx.doi.org/10.1016/j.stem.2008.01.002.
24. Aladjem MI, Spike BT, Rodewald LW, Hope TJ, Klemm M, Jaenisch R, et al. ES cells do not activate p53-dependent stress responses and undergo p53-independent apoptosis in response to DNA damage. Curr Biol 1998; 8:145-55; PMID:9443911; http://dx.doi.org/10.1016/S0960-9822(98)70061-2.
25. Qin H, Yu T, Qing T, Liu Y, Zhao Y, Cai J, et al. Regulation of apoptosis and differentiation by p53 in human embryonic stem cells. J Biol Chem 2007; 282:5842-52; PMID:17179143; http://dx.doi.org/10.1074/jbc.M610464200.
26. Solozobova V, Rolletschek A, Blattner C. Nuclear accumulation and activation of p53 in embryonic stem cells after DNA damage. BMC Cell Biol 2009; 10:46; PMID:19534768; http://dx.doi.org/10.1186/1471-2121-10-46.
27. Lin T, Chao C, Saito S, Mazur SJ, Murphy ME, Appella E, et al. p53 induces differentiation of mouse embryonic stem cells by suppressing Nanog expression. Nat Cell Biol 2005; 7:165-71; PMID:15619621; http://dx.doi.org/10. 1038/ncb1211.
28. Oliver TG, Meylan E, Chang GP, Xue W, Burke JR, Humpton TJ, et al. Caspase-2-mediated cleavage of Mdm2 creates a p53-induced positive feedback loop. Mol Cell 2011; 43:57-71; PMID:21726810; http://dx.doi.org/10.1016/j. molcel.2011.06.012.
29. Sasaki M, Kawahara K, Nishio M, Mimori K, Kogo R, Hamada K, et al. Regulation of the MDM2-p53 pathway and tumor growth by PICT1 via nucleolar RPL11. Nat Med 2011; 17:944-51; PMID:21804542; http://dx.doi.org/10.1038/nm. 2392.
30. 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; PMID:14609953; http://dx.doi.org/10.1093/emboj/cdg579.
31. Kurki S, Peltonen K, Latonen L, Kiviharju TM, Ojala PM, Meek D, et al. Nucleolar protein NPM interacts with HDM2 and protects tumor suppressor protein p53 from HDM2-mediated degradation. Cancer Cell 2004; 5:465-75; PMID:15144954; http://dx.doi.org/10.1016/S1535-6108(04)00110-2.
32. Al-Baker EA, Boyle J, Harry R, Kill IR. A p53-independent pathway regulates nucleolar segregation and antigen translocation in response to DNA damage induced by UV irradiation. Exp Cell Res 2004; 292:179-86; PMID:14720517; http://dx.doi.org/10.1016/j.yexcr.2003.09.006.
33. Li H, Collado M, Villasante A, Strati K, Ortega S, Cañamero M, et al. The Ink4/Arf locus is a barrier for iPS cell reprogramming. Nature 2009; 460:1136-9; PMID:19668188; http://dx.doi.org/10.1038/nature08290.