The Chromatin-Associated Phf12 Protein Maintains Nucleolar Integrity and Prevents Premature Cellular Senescence

REFERENCES

• Musselman CA, Kutateladze TG. 2011. Handpicking epigenetic marks with PHD fingers. Nucleic Acids Res 39:9061–9071. https://doi.org/10.1093/nar/gkr613.
   PubMed Web of Science ®Google Scholar
• Yochum GS, Ayer DE. 2001. Pf1, a novel PHD zinc finger protein that links the TLE corepressor to the mSin3A-histone deacetylase complex. Mol Cell Biol 21:4110–4118. https://doi.org/10.1128/MCB.21.13.4110-4118.2001.
   PubMedGoogle Scholar
• Hayakawa T, Ohtani Y, Hayakawa N, Shinmyozu K, Saito M, Ishikawa F, Nakayama J. 2007. RBP2 is an MRG15 complex component and down-regulates intragenic histone H3 lysine 4 methylation. Genes Cells 12:811–826.
   PubMed Web of Science ®Google Scholar
• Yochum GS, Ayer DE. 2002. Role for the mortality factors MORF4, MRGX, and MRG15 in transcriptional repression via associations with Pf1, mSin3A, and Transducin-Like Enhancer of Split. Mol Cell Biol 22:7868–7876. https://doi.org/10.1128/MCB.22.22.7868-7876.2002.
   PubMed Web of Science ®Google Scholar
• Xie T, Graveline R, Kumar GS, Zhang Y, Krishnan A, David G, Radhakrishnan I. 2012. Structural basis for molecular interactions involving MRG domains: implications in chromatin biology. Structure 20:151–160. https://doi.org/10.1016/j.str.2011.10.019.
   PubMedGoogle Scholar
• Jelinic P, Pellegrino J, David G. 2011. A novel mammalian complex containing Sin3B mitigates histone acetylation and RNA polymerase II progression within transcribed loci. Mol Cell Biol 31:54–62. https://doi.org/10.1128/MCB.00840-10.
   PubMed Web of Science ®Google Scholar
• Kaadige MR, Ayer DE. 2006. The polybasic region that follows the plant homeodomain zinc finger 1 of Pf1 is necessary and sufficient for specific phosphoinositide binding. J Biol Chem 281:28831–28836. https://doi.org/10.1074/jbc.M605624200.
   PubMed Web of Science ®Google Scholar
• Strobl-Mazzulla PH, Bronner ME. 2012. A PHD12-Snail2 repressive complex epigenetically mediates neural crest epithelial-to-mesenchymal transition. J Cell Biol 198:999–1010. https://doi.org/10.1083/jcb.201203098.
   PubMedGoogle Scholar
• Bansal N, Petrie K, Christova R, Chung CY, Leibovitch BA, Howell L, Gil V, Sbirkov Y, Lee E, Wexler J, Ariztia EV, Sharma R, Zhu J, Bernstein E, Zhou MM, Zelent A, Farias E, Waxman S. 2015. Targeting the SIN3A-PF1 interaction inhibits epithelial to mesenchymal transition and maintenance of a stem cell phenotype in triple negative breast cancer. Oncotarget 6:34087–34105. https://doi.org/10.18632/oncotarget.6048.
   PubMed Web of Science ®Google Scholar
• David G, Grandinetti KB, Finnerty PM, Simpson N, Chu GC, Depinho RA. 2008. Specific requirement of the chromatin modifier mSin3B in cell cycle exit and cellular differentiation. Proc Natl Acad Sci U S A 105:4168–4172. https://doi.org/10.1073/pnas.0710285105.
   PubMed Web of Science ®Google Scholar
• Grandinetti KB, David G. 2008. Sin3B: an essential regulator of chromatin modifications at E2F target promoters during cell cycle withdrawal. Cell Cycle 7:1550–1554. https://doi.org/10.4161/cc.7.11.6052.
   PubMed Web of Science ®Google Scholar
• Grandinetti KB, Jelinic P, DiMauro T, Pellegrino J, Fernandez Rodriguez R, Finnerty PM, Ruoff R, Bardeesy N, Logan SK, David G. 2009. Sin3B expression is required for cellular senescence and is up-regulated upon oncogenic stress. Cancer Res 69:6430–6437. https://doi.org/10.1158/0008-5472.CAN-09-0537.
   PubMed Web of Science ®Google Scholar
• Rielland M, Cantor DJ, Graveline R, Hajdu C, Mara L, Diaz BDD, Miller G, David G. 2014. Senescence-associated SIN3B promotes inflammation and pancreatic cancer progression. J Clin Invest 124:2125–2135. https://doi.org/10.1172/JCI72619.
   PubMed Web of Science ®Google Scholar
• Lagger G, O'Carroll D, Rembold M, Khier H, Tischler J, Weitzer G, Schuettengruber B, Hauser C, Brunmeir R, Jenuwein T, Seiser C. 2002. Essential function of histone deacetylase 1 in proliferation control and CDK inhibitor repression. EMBO J 21:2672–2681. https://doi.org/10.1093/emboj/21.11.2672.
   PubMed Web of Science ®Google Scholar
• Montgomery RL, Davis CA, Potthoff MJ, Haberland M, Fielitz J, Qi X, Hill JA, Richardson JA, Olson EN. 2007. Histone deacetylases 1 and 2 redundantly regulate cardiac morphogenesis, growth, and contractility. Genes Dev 21:1790–1802. https://doi.org/10.1101/gad.1563807.
   PubMed Web of Science ®Google Scholar
• Wilting RH, Yanover E, Heideman MR, Jacobs H, Horner J, van der Torre J, DePinho RA, Dannenberg JH. 2010. Overlapping functions of Hdac1 and Hdac2 in cell cycle regulation and haematopoiesis. EMBO J 29:2586–2597. https://doi.org/10.1038/emboj.2010.136.
   PubMed Web of Science ®Google Scholar
• Tominaga K, Kirtane B, Jackson JG, Ikeno Y, Ikeda T, Hawks C, Smith JR, Matzuk MM, Pereira-Smith OM. 2005. MRG15 regulates embryonic development and cell proliferation. Mol Cell Biol 25:2924–2937. https://doi.org/10.1128/MCB.25.8.2924-2937.2005.
   PubMedGoogle Scholar
• Di Micco R, Sulli G, Dobreva M, Liontos M, Botrugno OA, Gargiulo G, dal Zuffo R, Matti V, d'Ario G, Montani E, Mercurio C, Hahn WC, Gorgoulis V, Minucci S, d'Adda di Fagagna F. 2011. Interplay between oncogene-induced DNA damage response and heterochromatin in senescence and cancer. Nat Cell Biol 13:292–302. https://doi.org/10.1038/ncb2170.
   PubMed Web of Science ®Google Scholar
• Boisvert FM, van Koningsbruggen S, Navascues J, Lamond AI. 2007. The multifunctional nucleolus. Nat Rev Mol Cell Biol 8:574–585.
   PubMed Web of Science ®Google Scholar
• Holmberg Olausson K, Nister M, Lindstrom MS. 2012. p53-dependent and -independent nucleolar stress responses. Cells 1:774–798. https://doi.org/10.3390/cells1040774.
   PubMedGoogle Scholar
• Kar B, Liu B, Zhou Z, Lam YW. 2011. Quantitative nucleolar proteomics reveals nuclear re-organization during stress-induced senescence in mouse fibroblast. BMC Cell Biol 12:33. https://doi.org/10.1186/1471-2121-12-33.
   PubMedGoogle Scholar
• Sobol M, Yildirim S, Philimonenko VV, Marasek P, Castano E, Hozak P. 2013. UBF complexes with phosphatidylinositol 4,5-bisphosphate in nucleolar organizer regions regardless of ongoing RNA polymerase I activity. Nucleus 4:478–486. https://doi.org/10.4161/nucl.27154.
   PubMed Web of Science ®Google Scholar
• Newton K, Petfalski E, Tollervey D, Caceres JF. 2003. Fibrillarin is essential for early development and required for accumulation of an intron-encoded small nucleolar RNA in the mouse. Mol Cell Biol 23:8519–8527. https://doi.org/10.1128/MCB.23.23.8519-8527.2003.
   PubMed Web of Science ®Google Scholar
• Adams PD. 2007. Remodeling of chromatin structure in senescent cells and its potential impact on tumor suppression and aging. Gene 397:84–93. https://doi.org/10.1016/j.gene.2007.04.020.
   PubMed Web of Science ®Google Scholar
• Tollervey D, Lehtonen H, Jansen R, Kern H, Hurt EC. 1993. Temperature-sensitive mutations demonstrate roles for yeast fibrillarin in pre-rRNA processing, pre-rRNA methylation, and ribosome assembly. Cell 72:443–457. https://doi.org/10.1016/0092-8674(93)90120-F.
   PubMed Web of Science ®Google Scholar
• Finkbeiner E, Haindl M, Raman N, Muller S. 2011. SUMO routes ribosome maturation. Nucleus 2:527–532. https://doi.org/10.4161/nucl.2.6.17604.
   PubMed Web of Science ®Google Scholar
• Finkbeiner E, Haindl M, Muller S. 2011. The SUMO system controls nucleolar partitioning of a novel mammalian ribosome biogenesis complex. EMBO J 30:1067–1078. https://doi.org/10.1038/emboj.2011.33.
   PubMed Web of Science ®Google Scholar
• Grisendi S, Mecucci C, Falini B, Pandolfi PP. 2006. Nucleophosmin and cancer. Nat Rev Cancer 6:493–505. https://doi.org/10.1038/nrc1885.
   PubMed Web of Science ®Google Scholar
• Haindl M, Harasim T, Eick D, Muller S. 2008. The nucleolar SUMO-specific protease SENP3 reverses SUMO modification of nucleophosmin and is required for rRNA processing. EMBO Rep 9:273–279. https://doi.org/10.1038/embor.2008.3.
   PubMed Web of Science ®Google Scholar
• Raman N, Nayak A, Muller S. 2014. mTOR signaling regulates nucleolar targeting of the SUMO-specific isopeptidase SENP3. Mol Cell Biol 34:4474–4484. https://doi.org/10.1128/MCB.00801-14.
   PubMed Web of Science ®Google Scholar
• Kumar GS, Chang W, Xie T, Patel A, Zhang Y, Wang GG, David G, Radhakrishnan I. 2012. Sequence requirements for combinatorial recognition of histone H3 by the MRG15 and Pf1 subunits of the Rpd3S/Sin3S corepressor complex. J Mol Biol 422:519–531. https://doi.org/10.1016/j.jmb.2012.06.013.
   PubMed Web of Science ®Google Scholar
• Benevolenskaya EV, Murray HL, Branton P, Young RA, Kaelin WG, Jr. 2005. Binding of pRB to the PHD protein RBP2 promotes cellular differentiation. Mol Cell 18:623–635. https://doi.org/10.1016/j.molcel.2005.05.012.
   PubMed Web of Science ®Google Scholar
• Florens L, Carozza MJ, Swanson SK, Fournier M, Coleman MK, Workman JL, Washburn MP. 2006. Analyzing chromatin remodeling complexes using shotgun proteomics and normalized spectral abundance factors. Methods 40:303–311. https://doi.org/10.1016/j.ymeth.2006.07.028.
   PubMed Web of Science ®Google Scholar
• Mitchell L, Lambert JP, Gerdes M, Al-Madhoun AS, Skerjanc IS, Figeys D, Baetz K. 2008. Functional dissection of the NuA4 histone acetyltransferase reveals its role as a genetic hub and that Eaf1 is essential for complex integrity. Mol Cell Biol 28:2244–2256. https://doi.org/10.1128/MCB.01653-07.
   PubMed Web of Science ®Google Scholar
• Collado M. 2010. Exploring a ‘pro-senescence’ approach for prostate cancer therapy by targeting PTEN. Future Oncol 6:687–689. https://doi.org/10.2217/fon.10.39.
   PubMedGoogle Scholar
• Collado M, Serrano M. 2010. Senescence in tumours: evidence from mice and humans. Nat Rev Cancer 10:51–57. https://doi.org/10.1038/nrc2772.
   PubMed Web of Science ®Google Scholar
• Sharpless NE, Sherr CJ. 2015. Forging a signature of in vivo senescence. Nat Rev Cancer 15:397–408. https://doi.org/10.1038/nrc3960.
   PubMed Web of Science ®Google Scholar
• Dimauro T, David G. 2009. Chromatin modifications: the driving force of senescence and aging? Aging (Albany NY) 1:182–190.
   PubMedGoogle Scholar
• Kuilman T, Michaloglou C, Mooi WJ, Peeper DS. 2010. The essence of senescence. Genes Dev 24:2463–2479. https://doi.org/10.1101/gad.1971610.
   PubMed Web of Science ®Google Scholar
• Sinclair DA, Mills K, Guarente L. 1997. Accelerated aging and nucleolar fragmentation in yeast sgs1 mutants. Science 277:1313–1316. https://doi.org/10.1126/science.277.5330.1313.
   PubMed Web of Science ®Google Scholar
• van Deursen JM. 2014. The role of senescent cells in ageing. Nature 509:439–446. https://doi.org/10.1038/nature13193.
   PubMed Web of Science ®Google Scholar
• Nishimura K, Kumazawa T, Kuroda T, Katagiri N, Tsuchiya M, Goto N, Furumai R, Murayama A, Yanagisawa J, Kimura K. 2015. Perturbation of ribosome biogenesis drives cells into senescence through 5S RNP-mediated p53 activation. Cell Rep 10:1310–1323. https://doi.org/10.1016/j.celrep.2015.01.055.
   PubMed Web of Science ®Google Scholar
• Tsang CK, Bertram PG, Ai W, Drenan R, Zheng XF. 2003. Chromatin-mediated regulation of nucleolar structure and RNA Pol I localization by TOR. EMBO J 22:6045–6056. https://doi.org/10.1093/emboj/cdg578.
   PubMed Web of Science ®Google Scholar
• Zhou Y, Santoro R, Grummt I. 2002. The chromatin remodeling complex NoRC targets HDAC1 to the ribosomal gene promoter and represses RNA polymerase I transcription. EMBO J 21:4632–4640. https://doi.org/10.1093/emboj/cdf460.
   PubMed Web of Science ®Google Scholar
• Wong JC, Hasan MR, Rahman M, Yu AC, Chan SK, Schaeffer DF, Kennecke HF, Lim HJ, Owen D, Tai IT. 2013. Nucleophosmin 1, upregulated in adenomas and cancers of the colon, inhibits p53-mediated cellular senescence. Int J Cancer 133:1567–1577. https://doi.org/10.1002/ijc.28180.
   PubMed Web of Science ®Google Scholar
• Ning Z, Zhang Y, Chen H, Wu J, Song T, Wu Q, Liu F. 2014. PELP1 suppression inhibits colorectal cancer through c-Src downregulation. Oxid Med Cell Longev 2014:193523. https://doi.org/10.1155/2014/193523.
   PubMedGoogle Scholar
• Castle CD, Cassimere EK, Denicourt C. 2012. LAS1L interacts with the mammalian Rix1 complex to regulate ribosome biogenesis. Mol Biol Cell 23:716–728. https://doi.org/10.1091/mbc.E11-06-0530.
   PubMed Web of Science ®Google Scholar
• Calo E, Flynn RA, Martin L, Spitale RC, Chang HY, Wysocka J. 2015. RNA helicase DDX21 coordinates transcription and ribosomal RNA processing. Nature 518:249–253. https://doi.org/10.1038/nature13923.
   PubMed Web of Science ®Google Scholar
• Serrano M, Lin AW, McCurrach ME, Beach D, Lowe SW. 1997. Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell 88:593–602. https://doi.org/10.1016/S0092-8674(00)81902-9.
   PubMed Web of Science ®Google Scholar
• Reich M, Liefeld T, Gould J, Lerner J, Tamayo P, Mesirov JP. 2006. GenePattern 2.0. Nat Genet 38:500–501. https://doi.org/10.1038/ng0506-500.
   PubMed Web of Science ®Google Scholar
• Huang DW, Sherman BT, Lempicki RA. 2009. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4:44–57. https://doi.org/10.1038/nprot.2008.211.
   PubMed Web of Science ®Google Scholar
• Huang DW, Sherman BT, Zheng X, Yang J, Imamichi T, Stephens R, Lempicki RA. 2009. Extracting biological meaning from large gene lists with DAVID. Curr Protoc Bioinformatics 27:13.11.1–13.11.13. https://doi.org/10.1002/0471250953.bi1311s27.
   Google Scholar
• Cotto-Rios XM, Bekes M, Chapman J, Ueberheide B, Huang TT. 2012. Deubiquitinases as a signaling target of oxidative stress. Cell Rep 2:1475–1484. https://doi.org/10.1016/j.celrep.2012.11.011.
   PubMed Web of Science ®Google Scholar