MDM2 Mediates Nonproteolytic Polyubiquitylation of the DEAD-Box RNA Helicase DDX24

REFERENCES

• Brooks CL, Gu W. 2006. p53 ubiquitination: Mdm2 and beyond. Mol. Cell 21:307–315. http://dx.doi.org/10.1016/j.molcel.2006.01.020.
   PubMed Web of Science ®Google Scholar
• Marine JC, Lozano G. 2010. Mdm2-mediated ubiquitylation: p53 and beyond. Cell Death Differ. 17:93–102. http://dx.doi.org/10.1038/cdd.2009.68.
   PubMed Web of Science ®Google Scholar
• Momand J, Zambetti GP, Olson DC, George D, Levine AJ. 1992. The mdm-2 oncogene product forms a complex with the p53 protein and inhibits p53-mediated transactivation. Cell 69:1237–1245. http://dx.doi.org/10.1016/0092-8674(92)90644-R.
   PubMed Web of Science ®Google Scholar
• Oliner JD, Pietenpol JA, Thiagalingam S, Gyuris J, Kinzler KW, Vogelstein B. 1993. Oncoprotein MDM2 conceals the activation domain of tumour suppressor p53. Nature 362:857–860. http://dx.doi.org/10.1038/362857a0.
   PubMed Web of Science ®Google Scholar
• Haupt Y, Maya R, Kazaz A, Oren M. 1997. Mdm2 promotes the rapid degradation of p53. Nature 387:296–299. http://dx.doi.org/10.1038/387296a0.
   PubMed Web of Science ®Google Scholar
• Honda R, Tanaka H, Yasuda H. 1997. Oncoprotein MDM2 is a ubiquitin ligase E3 for tumor suppressor p53. FEBS Lett. 420:25–27. http://dx.doi.org/10.1016/S0014-5793(97)01480-4.
   PubMed Web of Science ®Google Scholar
• Kubbutat MH, Jones SN, Vousden KH. 1997. Regulation of p53 stability by Mdm2. Nature 387:299–303. http://dx.doi.org/10.1038/387299a0.
   PubMed Web of Science ®Google Scholar
• Barak Y, Juven T, Haffner R, Oren M. 1993. mdm2 expression is induced by wild type p53 activity. EMBO J. 12:461–468.
   PubMed Web of Science ®Google Scholar
• Juven T, Barak Y, Zauberman A, George DL, Oren M. 1993. Wild type p53 can mediate sequence-specific transactivation of an internal promoter within the mdm2 gene. Oncogene 8:3411–3416.
   PubMed Web of Science ®Google Scholar
• Boulon S, Westman BJ, Hutten S, Boisvert FM, Lamond AI. 2010. The nucleolus under stress. Mol. Cell 40:216–227. http://dx.doi.org/10.1016/j.molcel.2010.09.024.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Lu H. 2009. Signaling to p53: ribosomal proteins find their way. Cancer Cell 16:369–377. http://dx.doi.org/10.1016/j.ccr.2009.09.024.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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. http://dx.doi.org/10.1016/S1535-6108(03)00134-X.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Wolf GW, Bhat K, Jin A, Allio T, Burkhart WA, Xiong Y. 2003. Ribosomal protein L11 negatively regulates oncoprotein MDM2 and mediates a p53-dependent ribosomal-stress checkpoint pathway. Mol. Cell. Biol. 23:8902–8912. http://dx.doi.org/10.1128/MCB.23.23.8902-8912.2003.
   PubMed Web of Science ®Google Scholar
• Bhat KP, Itahana K, Jin A, Zhang Y. 2004. Essential role of ribosomal protein L11 in mediating growth inhibition-induced p53 activation. EMBO J. 23:2402–2412. http://dx.doi.org/10.1038/sj.emboj.7600247.
   PubMed Web of Science ®Google Scholar
• Dai MS, Lu H. 2004. Inhibition of MDM2-mediated p53 ubiquitination and degradation by ribosomal protein L5. J. Biol. Chem. 279:44475–44482. http://dx.doi.org/10.1074/jbc.M403722200.
   PubMed Web of Science ®Google Scholar
• Dai MS, Zeng SX, Jin Y, Sun XX, David L, Lu H. 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. http://dx.doi.org/10.1128/MCB.24.17.7654-7668.2004.
   PubMed Web of Science ®Google Scholar
• 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. http://dx.doi.org/10.1128/MCB.24.17.7669-7680.2004.
   PubMed Web of Science ®Google Scholar
• Deisenroth C, Zhang Y. 2010. Ribosome biogenesis surveillance: probing the ribosomal protein-Mdm2-p53 pathway. Oncogene 29:4253–4260. http://dx.doi.org/10.1038/onc.2010.189.
   PubMed Web of Science ®Google Scholar
• Grummt I. 2003. Life on a planet of its own: regulation of RNA polymerase I transcription in the nucleolus. Genes Dev. 17:1691–1702. http://dx.doi.org/10.1101/gad.1098503R.
   PubMed Web of Science ®Google Scholar
• Henras AK, Soudet J, Gerus M, Lebaron S, Caizergues-Ferrer M, Mougin A, Henry Y. 2008. The post-transcriptional steps of eukaryotic ribosome biogenesis. Cell. Mol. Life Sci. 65:2334–2359. http://dx.doi.org/10.1007/s00018-008-8027-0.
   PubMed Web of Science ®Google Scholar
• Mullineux ST, Lafontaine DL. 2012. Mapping the cleavage sites on mammalian pre-rRNAs: where do we stand? Biochimie 94:1521–1532. http://dx.doi.org/10.1016/j.biochi.2012.02.001.
   PubMed Web of Science ®Google Scholar
• Staley JP, Woolford JLJr. 2009. Assembly of ribosomes and spliceosomes: complex ribonucleoprotein machines. Curr. Opin. Cell Biol. 21:109–118. http://dx.doi.org/10.1016/j.ceb.2009.01.003.
   PubMedGoogle Scholar
• Takahashi N, Yanagida M, Fujiyama S, Hayano T, Isobe T. 2003. Proteomic snapshot analyses of preribosomal ribonucleoprotein complexes formed at various stages of ribosome biogenesis in yeast and mammalian cells. Mass Spectrom. Rev. 22:287–317. http://dx.doi.org/10.1002/mas.10057.
   PubMedGoogle Scholar
• Orru S, Aspesi A, Armiraglio M, Caterino M, Loreni F, Ruoppolo M, Santoro C, Dianzani I. 2007. Analysis of the ribosomal protein S19 interactome. Mol. Cell. Proteomics 6:382–393. http://dx.doi.org/10.1074/mcp.M600156-MCP200.
   PubMedGoogle Scholar
• Fujiyama-Nakamura S, Yoshikawa H, Homma K, Hayano T, Tsujimura-Takahashi T, Izumikawa K, Ishikawa H, Miyazawa N, Yanagida M, Miura Y, Shinkawa T, Yamauchi Y, Isobe T, Takahashi N. 2009. Parvulin (Par14), a peptidyl-prolyl cis-trans isomerase, is a novel rRNA processing factor that evolved in the metazoan lineage. Mol. Cell. Proteomics 8:1552–1565. http://dx.doi.org/10.1074/mcp.M900147-MCP200.
   PubMedGoogle Scholar
• Simabuco FM, Morello LG, Aragao AZ, Paes Leme AF, Zanchin NI. 2012. Proteomic characterization of the human FTSJ3 preribosomal complexes. J. Proteome Res. 11:3112–3126. http://dx.doi.org/10.1021/pr201106n.
   PubMed Web of Science ®Google Scholar
• Bleichert F, Baserga SJ. 2007. The long unwinding road of RNA helicases. Mol. Cell 27:339–352. http://dx.doi.org/10.1016/j.molcel.2007.07.014.
   PubMed Web of Science ®Google Scholar
• Linder P, Jankowsky E. 2011. From unwinding to clamping—the DEAD box RNA helicase family. Nat. Rev. Mol. Cell Biol. 12:505–516. http://dx.doi.org/10.1038/nrm3154.
   PubMed Web of Science ®Google Scholar
• Zagulski M, Kressler D, Becam AM, Rytka J, Herbert CJ. 2003. Mak5p, which is required for the maintenance of the M1 dsRNA virus, is encoded by the yeast ORF YBR142w and is involved in the biogenesis of the 60S subunit of the ribosome. Mol. Genet. Genomics 270:216–224. http://dx.doi.org/10.1007/s00438-003-0913-4.
   PubMed Web of Science ®Google Scholar
• Kitagawa M, Hatakeyama S, Shirane M, Matsumoto M, Ishida N, Hattori K, Nakamichi I, Kikuchi A, Nakayama KI, Nakayama K. 1999. An F-box protein, FWD1, mediates ubiquitin-dependent proteolysis of β-catenin. EMBO J. 18:2401–2410. http://dx.doi.org/10.1093/emboj/18.9.2401.
   PubMed Web of Science ®Google Scholar
• Kamura T, Hara T, Kotoshiba S, Yada M, Ishida N, Imaki H, Hatakeyama S, Nakayama K, Nakayama KI. 2003. Degradation of p57Kip2 mediated by SCFSkp2-dependent ubiquitylation. Proc. Natl. Acad. Sci. U. S. A. 100:10231–10236. http://dx.doi.org/10.1073/pnas.1831009100.
   PubMed Web of Science ®Google Scholar
• Jirawatnotai S, Hu Y, Michowski W, Elias JE, Becks L, Bienvenu F, Zagozdzon A, Goswami T, Wang YE, Clark AB, Kunkel TA, van Harn T, Xia B, Correll M, Quackenbush J, Livingston DM, Gygi SP, Sicinski P. 2011. A function for cyclin D1 in DNA repair uncovered by protein interactome analyses in human cancers. Nature 474:230–234. http://dx.doi.org/10.1038/nature10155.
   PubMed Web of Science ®Google Scholar
• Yada M, Hatakeyama S, Kamura T, Nishiyama M, Tsunematsu R, Imaki H, Ishida N, Okumura F, Nakayama K, Nakayama KI. 2004. Phosphorylation-dependent degradation of c-Myc is mediated by the F-box protein Fbw7. EMBO J. 23:2116–2125. http://dx.doi.org/10.1038/sj.emboj.7600217.
   PubMed Web of Science ®Google Scholar
• Tahara-Hanaoka S, Sudo K, Ema H, Miyoshi H, Nakauchi H. 2002. Lentiviral vector-mediated transduction of murine CD34(–) hematopoietic stem cells. Exp. Hematol. 30:11–17. http://dx.doi.org/10.1016/S0301-472X(01)00761-5.
   PubMedGoogle Scholar
• Kobayashi Y, Yonehara S. 2009. Novel cell death by downregulation of eEF1A1 expression in tetraploids. Cell Death Differ. 16:139–150. http://dx.doi.org/10.1038/cdd.2008.136.
   PubMedGoogle Scholar
• Hershko A, Heller H. 1985. Occurrence of a polyubiquitin structure in ubiquitin-protein conjugates. Biochem. Biophys. Res. Commun. 128:1079–1086. http://dx.doi.org/10.1016/0006-291X(85)91050-2.
   PubMed Web of Science ®Google Scholar
• Morello LG, Hesling C, Coltri PP, Castilho BA, Rimokh R, Zanchin NI. 2011. The NIP7 protein is required for accurate pre-rRNA processing in human cells. Nucleic Acids Res. 39:648–665. http://dx.doi.org/10.1093/nar/gkq758.
   PubMedGoogle Scholar
• Klibanov SA, O'Hagan HM, Ljungman M. 2001. Accumulation of soluble and nucleolar-associated p53 proteins following cellular stress. J. Cell Sci. 114:1867–1873.
   PubMedGoogle Scholar
• Latonen L, Kurki S, Pitkanen K, Laiho M. 2003. p53 and MDM2 are regulated by PI-3-kinases on multiple levels under stress induced by UV radiation and proteasome dysfunction. Cell. Signal. 15:95–102. http://dx.doi.org/10.1016/S0898-6568(02)00044-X.
   PubMedGoogle Scholar
• Dai MS, Sun XX, Lu H. 2008. Aberrant expression of nucleostemin activates p53 and induces cell cycle arrest via inhibition of MDM2. Mol. Cell. Biol. 28:4365–4376. http://dx.doi.org/10.1128/MCB.01662-07.
   PubMed Web of Science ®Google Scholar
• Lessard F, Stefanovsky V, Tremblay MG, Moss T. 2012. The cellular abundance of the essential transcription termination factor TTF-I regulates ribosome biogenesis and is determined by MDM2 ubiquitinylation. Nucleic Acids Res. 40:5357–5367. http://dx.doi.org/10.1093/nar/gks198.
   PubMed Web of Science ®Google Scholar
• Manfredi JJ. 2010. The Mdm2-p53 relationship evolves: Mdm2 swings both ways as an oncogene and a tumor suppressor. Genes Dev. 24:1580–1589. http://dx.doi.org/10.1101/gad.1941710.
   PubMed Web of Science ®Google Scholar
• Ye Y, Rape M. 2009. Building ubiquitin chains: E2 enzymes at work. Nat. Rev. Mol. Cell Biol. 10:755–764. http://dx.doi.org/10.1038/nrm2780.
   PubMed Web of Science ®Google Scholar
• van Wijk SJ, Timmers HT. 2010. The family of ubiquitin-conjugating enzymes (E2s): deciding between life and death of proteins. FASEB J. 24:981–993. http://dx.doi.org/10.1096/fj.09-136259.
   PubMedGoogle Scholar
• Shloush J, Vlassov JE, Engson I, Duan S, Saridakis V, Dhe-Paganon S, Raught B, Sheng Y, Arrowsmith CH. 2011. Structural and functional comparison of the RING domains of two p53 E3 ligases, Mdm2 and Pirh2. J. Biol. Chem. 286:4796–4808. http://dx.doi.org/10.1074/jbc.M110.157669.
   PubMedGoogle Scholar
• Rinaldo C, Prodosmo A, Mancini F, Iacovelli S, Sacchi A, Moretti F, Soddu S. 2007. MDM2-regulated degradation of HIPK2 prevents p53Ser46 phosphorylation and DNA damage-induced apoptosis. Mol. Cell 25:739–750. http://dx.doi.org/10.1016/j.molcel.2007.02.008.
   PubMed Web of Science ®Google Scholar
• 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. http://dx.doi.org/10.1016/j.molcel.2008.08.031.
   PubMed Web of Science ®Google Scholar
• Sloan KE, Mattijssen S, Lebaron S, Tollervey D, Pruijn GJ, Watkins NJ. 2013. Both endonucleolytic and exonucleolytic cleavage mediate ITS1 removal during human ribosomal RNA processing. J. Cell Biol. 200:577–588. http://dx.doi.org/10.1083/jcb.201207131.
   PubMed Web of Science ®Google Scholar
• Chen ZJ, Sun LJ. 2009. Nonproteolytic functions of ubiquitin in cell signaling. Mol. Cell 33:275–286. http://dx.doi.org/10.1016/j.molcel.2009.01.014.
   PubMed Web of Science ®Google Scholar
• Trempe JF. 2011. Reading the ubiquitin postal code. Curr. Opin. Struct. Biol. 21:792–801. http://dx.doi.org/10.1016/j.sbi.2011.09.009.
   PubMed Web of Science ®Google Scholar
• Ginisty H, Amalric F, Bouvet P. 1998. Nucleolin functions in the first step of ribosomal RNA processing. EMBO J. 17:1476–1486. http://dx.doi.org/10.1093/emboj/17.5.1476.
   PubMed Web of Science ®Google Scholar
• Zanchin NI, Goldfarb DS. 1999. Nip7p interacts with Nop8p, an essential nucleolar protein required for 60S ribosome biogenesis, and the exosome subunit Rrp43p. Mol. Cell. Biol. 19:1518–1525.
   PubMedGoogle Scholar
• Li M, Brooks CL, Wu-Baer F, Chen D, Baer R, Gu W. 2003. Mono- versus polyubiquitination: differential control of p53 fate by Mdm2. Science 302:1972–1975. http://dx.doi.org/10.1126/science.1091362.
   PubMed Web of Science ®Google Scholar
• Tafforeau L, Zorbas C, Langhendries JL, Mullineux ST, Stamatopoulou V, Mullier R, Wacheul L, Lafontaine DL. 2013. The complexity of human ribosome biogenesis revealed by systematic nucleolar screening of pre-rRNA processing factors. Mol. Cell 51:539–551. http://dx.doi.org/10.1016/j.molcel.2013.08.011.
   PubMed Web of Science ®Google Scholar
• Minsky N, Oren M. 2004. The RING domain of Mdm2 mediates histone ubiquitylation and transcriptional repression. Mol. Cell 16:631–639. http://dx.doi.org/10.1016/j.molcel.2004.10.016.
   PubMed Web of Science ®Google Scholar
• Maguire M, Nield PC, Devling T, Jenkins RE, Park BK, Polanski R, Vlatkovic N, Boyd MT. 2008. MDM2 regulates dihydrofolate reductase activity through monoubiquitination. Cancer Res. 68:3232–3242. http://dx.doi.org/10.1158/0008-5472.CAN-07-5271.
   PubMedGoogle Scholar
• Brenkman AB, de Keizer PL, van den Broek NJ, Jochemsen AG, Burgering BM. 2008. Mdm2 induces mono-ubiquitination of FOXO4. PLoS One 3:e2819. http://dx.doi.org/10.1371/journal.pone.0002819.
   PubMedGoogle Scholar
• Komander D, Rape M. 2012. The ubiquitin code. Annu. Rev. Biochem. 81:203–229. http://dx.doi.org/10.1146/annurev-biochem-060310-170328.
   PubMed Web of Science ®Google Scholar
• Kulathu Y, Komander D. 2012. Atypical ubiquitylation—the unexplored world of polyubiquitin beyond Lys48 and Lys63 linkages. Nat. Rev. Mol. Cell Biol. 13:508–523. http://dx.doi.org/10.1038/nrm3394.
   PubMed Web of Science ®Google Scholar
• Thrower JS, Hoffman L, Rechsteiner M, Pickart CM. 2000. Recognition of the polyubiquitin proteolytic signal. EMBO J. 19:94–102. http://dx.doi.org/10.1093/emboj/19.1.94.
   PubMed Web of Science ®Google Scholar
• Kim HT, Kim KP, Lledias F, Kisselev AF, Scaglione KM, Skowyra D, Gygi SP, Goldberg AL. 2007. Certain pairs of ubiquitin-conjugating enzymes (E2s) and ubiquitin-protein ligases (E3s) synthesize nondegradable forked ubiquitin chains containing all possible isopeptide linkages. J. Biol. Chem. 282:17375–17386. http://dx.doi.org/10.1074/jbc.M609659200.
   PubMed Web of Science ®Google Scholar
• Kim HT, Kim KP, Uchiki T, Gygi SP, Goldberg AL. 2009. S5a promotes protein degradation by blocking synthesis of nondegradable forked ubiquitin chains. EMBO J. 28:1867–1877. http://dx.doi.org/10.1038/emboj.2009.115.
   PubMedGoogle Scholar
• Ziv I, Kleifeld O, Glickman M. 2009. Nonconformity in ubiquitin compliance. EMBO J. 28:1825–1827. http://dx.doi.org/10.1038/emboj.2009.132.
   PubMedGoogle Scholar
• Yanagida M, Shimamoto A, Nishikawa K, Furuichi Y, Isobe T, Takahashi N. 2001. Isolation and proteomic characterization of the major proteins of the nucleolin-binding ribonucleoprotein complexes. Proteomics 1:1390–1404. http://dx.doi.org/10.1002/1615-9861(200111)1:11<1390::AID-PROT1390>3.0.CO;2-Z.
   PubMed Web of Science ®Google Scholar
• Hayano T, Yanagida M, Yamauchi Y, Shinkawa T, Isobe T, Takahashi N. 2003. Proteomic analysis of human Nop56p-associated pre-ribosomal ribonucleoprotein complexes. Possible link between Nop56p and the nucleolar protein treacle responsible for Treacher Collins syndrome. J. Biol. Chem. 278:34309–34319. http://dx.doi.org/10.1074/jbc.M304304200.
   PubMed Web of Science ®Google Scholar
• Lindstrom MS, Zhang Y. 2008. Ribosomal protein S9 is a novel B23/NPM-binding protein required for normal cell proliferation. J. Biol. Chem. 283:15568–15576. http://dx.doi.org/10.1074/jbc.M801151200.
   PubMed Web of Science ®Google Scholar
• Maggi LBJr, Kuchenruether M, Dadey DY, Schwope RM, Grisendi S, Townsend RR, Pandolfi PP, Weber JD. 2008. Nucleophosmin serves as a rate-limiting nuclear export chaperone for the mammalian ribosome. Mol. Cell. Biol. 28:7050–7065. http://dx.doi.org/10.1128/MCB.01548-07.
   PubMed Web of Science ®Google Scholar
• Coute Y, Kindbeiter K, Belin S, Dieckmann R, Duret L, Bezin L, Sanchez JC, Diaz JJ. 2008. ISG20L2, a novel vertebrate nucleolar exoribonuclease involved in ribosome biogenesis. Mol. Cell. Proteomics 7:546–559. http://dx.doi.org/10.1074/mcp.M700510-MCP200.
   PubMedGoogle Scholar
• Ball HL, Zhang B, Riches JJ, Gandhi R, Li J, Rommens JM, Myers JS. 2009. Shwachman-Bodian Diamond syndrome is a multi-functional protein implicated in cellular stress responses. Hum. Mol. Genet. 18:3684–3695. http://dx.doi.org/10.1093/hmg/ddp316.
   PubMed Web of Science ®Google Scholar
• Borer RA, Lehner CF, Eppenberger HM, Nigg EA. 1989. Major nucleolar proteins shuttle between nucleus and cytoplasm. Cell 56:379–390. http://dx.doi.org/10.1016/0092-8674(89)90241-9.
   PubMed Web of Science ®Google Scholar
• Bouvet P, Diaz JJ, Kindbeiter K, Madjar JJ, Amalric F. 1998. Nucleolin interacts with several ribosomal proteins through its RGG domain. J. Biol. Chem. 273:19025–19029. http://dx.doi.org/10.1074/jbc.273.30.19025.
   PubMed Web of Science ®Google Scholar
• Panse VG, Kressler D, Pauli A, Petfalski E, Gnadig M, Tollervey D, Hurt E. 2006. Formation and nuclear export of preribosomes are functionally linked to the small-ubiquitin-related modifier pathway. Traffic 7:1311–1321. http://dx.doi.org/10.1111/j.1600-0854.2006.00471.x.
   PubMed Web of Science ®Google Scholar
• Kressler D, Roser D, Pertschy B, Hurt E. 2008. The AAA ATPase Rix7 powers progression of ribosome biogenesis by stripping Nsa1 from pre-60S particles. J. Cell Biol. 181:935–944. http://dx.doi.org/10.1083/jcb.200801181.
   PubMed Web of Science ®Google Scholar
• Strunk BS, Karbstein K. 2009. Powering through ribosome assembly. RNA 15:2083–2104. http://dx.doi.org/10.1261/rna.1792109.
   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. http://dx.doi.org/10.1038/emboj.2011.33.
   PubMed Web of Science ®Google Scholar