Impaired ribosome biogenesis: mechanisms and relevance to cancer and aging
Jazyk angličtina Země Spojené státy americké Médium print
Typ dokumentu časopisecké články, práce podpořená grantem, přehledy
PubMed
31026227
PubMed Central
PMC6520011
DOI
10.18632/aging.101922
PII: 101922
Knihovny.cz E-zdroje
- Klíčová slova
- aging, cancer, p53, ribosome biogenesis, ribosomopathy,
- MeSH
- biogeneze organel MeSH
- lidé MeSH
- nádory metabolismus MeSH
- ribozomální proteiny metabolismus MeSH
- ribozomy metabolismus MeSH
- stárnutí metabolismus MeSH
- zvířata MeSH
- Check Tag
- lidé MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- přehledy MeSH
- Názvy látek
- ribozomální proteiny MeSH
The biosynthesis of ribosomes is a complex process that requires the coordinated action of many factors and a huge energy investment from the cell. Ribosomes are essential for protein production, and thus for cellular survival, growth and proliferation. Ribosome biogenesis is initiated in the nucleolus and includes: the synthesis and processing of ribosomal RNAs, assembly of ribosomal proteins, transport to the cytoplasm and association of ribosomal subunits. The disruption of ribosome biogenesis at various steps, with either increased or decreased expression of different ribosomal components, can promote cell cycle arrest, senescence or apoptosis. Additionally, interference with ribosomal biogenesis is often associated with cancer, aging and age-related degenerative diseases. Here, we review current knowledge on impaired ribosome biogenesis, discuss the main factors involved in stress responses under such circumstances and focus on examples with clinical relevance.
Zobrazit více v PubMed
Rudra D, Warner JR. What better measure than ribosome synthesis? Genes Dev. 2004; 18:2431–36. 10.1101/gad.1256704 PubMed DOI
McStay B. Nucleolar organizer regions: genomic ‘dark matter’ requiring illumination. Genes Dev. 2016; 30:1598–610. 10.1101/gad.283838.116 PubMed DOI PMC
Henras AK, Plisson-Chastang C, O’Donohue MF, Chakraborty A, Gleizes PE. An overview of pre-ribosomal RNA processing in eukaryotes. Wiley Interdiscip Rev RNA. 2015; 6:225–42. 10.1002/wrna.1269 PubMed DOI PMC
Sørensen PD, Frederiksen S. Characterization of human 5S rRNA genes. Nucleic Acids Res. 1991; 19:4147–51. 10.1093/nar/19.15.4147 PubMed DOI PMC
Paule MR, White RJ. Survey and summary: transcription by RNA polymerases I and III. Nucleic Acids Res. 2000; 28:1283–98. 10.1093/nar/28.6.1283 PubMed DOI PMC
Wang W, Nag S, Zhang X, Wang MH, Wang H, Zhou J, Zhang R. Ribosomal proteins and human diseases: pathogenesis, molecular mechanisms, and therapeutic implications. Med Res Rev. 2015; 35:225–85. 10.1002/med.21327 PubMed DOI PMC
Fromont-Racine M, Senger B, Saveanu C, Fasiolo F. Ribosome assembly in eukaryotes. Gene. 2003; 313:17–42. 10.1016/S0378-1119(03)00629-2 PubMed DOI
Golomb L, Volarevic S, Oren M. p53 and ribosome biogenesis stress: the essentials. FEBS Lett. 2014; 588:2571–79. 10.1016/j.febslet.2014.04.014 PubMed DOI
Grummt I. Life on a planet of its own: regulation of RNA polymerase I transcription in the nucleolus. Genes Dev. 2003; 17:1691–702. 10.1101/gad.1098503R PubMed DOI
Grummt I. Wisely chosen paths--regulation of rRNA synthesis: delivered on 30 June 2010 at the 35th FEBS Congress in Gothenburg, Sweden. FEBS J. 2010; 277:4626–39. 10.1111/j.1742-4658.2010.07892.x PubMed DOI
James A, Wang Y, Raje H, Rosby R, DiMario P. Nucleolar stress with and without p53. Nucleus. 2014; 5:402–26. 10.4161/nucl.32235 PubMed DOI PMC
Volarević S, Stewart MJ, Ledermann B, Zilberman F, Terracciano L, Montini E, Grompe M, Kozma SC, Thomas G. Proliferation, but not growth, blocked by conditional deletion of 40S ribosomal protein S6. Science. 2000; 288:2045–47. 10.1126/science.288.5473.2045 PubMed DOI
Gentilella A, Morón-Duran FD, Fuentes P, Zweig-Rocha G, Riaño-Canalias F, Pelletier J, Ruiz M, Turón G, Castaño J, Tauler A, Bueno C, Menéndez P, Kozma SC, Thomas G. Autogenous Control of 5′TOP mRNA Stability by 40S Ribosomes. Mol Cell. 2017; 67:55–70.e4. 10.1016/j.molcel.2017.06.005 PubMed DOI PMC
Hariharan N, Sussman MA. Stressing on the nucleolus in cardiovascular disease. Biochim Biophys Acta. 2014; 1842:798–801. 10.1016/j.bbadis.2013.09.016 PubMed DOI PMC
Salvetti A, Greco A. Viruses and the nucleolus: the fatal attraction. Biochim Biophys Acta. 2014; 1842:840–47. 10.1016/j.bbadis.2013.12.010 PubMed DOI PMC
Parlato R, Liss B. How Parkinson’s disease meets nucleolar stress. Biochim Biophys Acta. 2014; 1842:791–97. 10.1016/j.bbadis.2013.12.014 PubMed DOI
Hetman M, Pietrzak M. Emerging roles of the neuronal nucleolus. Trends Neurosci. 2012; 35:305–14. 10.1016/j.tins.2012.01.002 PubMed DOI PMC
Montanaro L, Treré D, Derenzini M. Nucleolus, ribosomes, and cancer. Am J Pathol. 2008; 173:301–10. 10.2353/ajpath.2008.070752 PubMed DOI PMC
Zink D, Fischer AH, Nickerson JA. Nuclear structure in cancer cells. Nat Rev Cancer. 2004; 4:677–87. 10.1038/nrc1430 PubMed DOI
Armistead J, Triggs-Raine B. Diverse diseases from a ubiquitous process: the ribosomopathy paradox. FEBS Lett. 2014; 588:1491–500. 10.1016/j.febslet.2014.03.024 PubMed DOI
Danilova N, Gazda HT. Ribosomopathies: how a common root can cause a tree of pathologies. Dis Model Mech. 2015; 8:1013–26. 10.1242/dmm.020529 PubMed DOI PMC
Russell J, Zomerdijk JC. RNA-polymerase-I-directed rDNA transcription, life and works. Trends Biochem Sci. 2005; 30:87–96. 10.1016/j.tibs.2004.12.008 PubMed DOI PMC
Albert B, Perez-Fernandez J, Léger-Silvestre I, Gadal O. Regulation of ribosomal RNA production by RNA polymerase I: does elongation come first? Genet Res Int. 2012; 2012:276948. 10.1155/2012/276948 PubMed DOI PMC
O’Sullivan AC, Sullivan GJ, McStay B. UBF binding in vivo is not restricted to regulatory sequences within the vertebrate ribosomal DNA repeat. Mol Cell Biol. 2002; 22:657–68. 10.1128/MCB.22.2.657-668.2002 PubMed DOI PMC
Jansa P, Grummt I. Mechanism of transcription termination: PTRF interacts with the largest subunit of RNA polymerase I and dissociates paused transcription complexes from yeast and mouse. Mol Gen Genet. 1999; 262:508–14. 10.1007/s004380051112 PubMed DOI
Ciganda M, Williams N. Eukaryotic 5S rRNA biogenesis. Wiley Interdiscip Rev RNA. 2011; 2:523–33. 10.1002/wrna.74 PubMed DOI PMC
Stefanovsky V, Langlois F, Gagnon-Kugler T, Rothblum LI, Moss T. Growth factor signaling regulates elongation of RNA polymerase I transcription in mammals via UBF phosphorylation and r-chromatin remodeling. Mol Cell. 2006; 21:629–39. 10.1016/j.molcel.2006.01.023 PubMed DOI
Stefanovsky VY, Moss T. The splice variants of UBF differentially regulate RNA polymerase I transcription elongation in response to ERK phosphorylation. Nucleic Acids Res. 2008; 36:5093–101. 10.1093/nar/gkn484 PubMed DOI PMC
Zhao J, Yuan X, Frödin M, Grummt I. ERK-dependent phosphorylation of the transcription initiation factor TIF-IA is required for RNA polymerase I transcription and cell growth. Mol Cell. 2003; 11:405–13. 10.1016/S1097-2765(03)00036-4 PubMed DOI
Felton-Edkins ZA, Fairley JA, Graham EL, Johnston IM, White RJ, Scott PH. The mitogen-activated protein (MAP) kinase ERK induces tRNA synthesis by phosphorylating TFIIIB. EMBO J. 2003; 22:2422–32. 10.1093/emboj/cdg240 PubMed DOI PMC
Zhu J, Blenis J, Yuan J. Activation of PI3K/Akt and MAPK pathways regulates Myc-mediated transcription by phosphorylating and promoting the degradation of Mad1. Proc Natl Acad Sci USA. 2008; 105:6584–89. 10.1073/pnas.0802785105 PubMed DOI PMC
Mendoza MC, Er EE, Blenis J. The Ras-ERK and PI3K-mTOR pathways: cross-talk and compensation. Trends Biochem Sci. 2011; 36:320–28. 10.1016/j.tibs.2011.03.006 PubMed DOI PMC
Gomez-Roman N, Felton-Edkins ZA, Kenneth NS, Goodfellow SJ, Athineos D, Zhang J, Ramsbottom BA, Innes F, Kantidakis T, Kerr ER, Brodie J, Grandori C, White RJ. Activation by c-Myc of transcription by RNA polymerases I, II and III. Biochem Soc Symp. 2006; 73:141–54. 10.1042/bss0730141 PubMed DOI
van Riggelen J, Yetil A, Felsher DW. MYC as a regulator of ribosome biogenesis and protein synthesis. Nat Rev Cancer. 2010; 10:301–09. 10.1038/nrc2819 PubMed DOI
White RJ. RNA polymerases I and III, growth control and cancer. Nat Rev Mol Cell Biol. 2005; 6:69–78. 10.1038/nrm1551 PubMed DOI
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. 10.1038/sj.onc.1209883 PubMed DOI
Woiwode A, Johnson SA, Zhong S, Zhang C, Roeder RG, Teichmann M, Johnson DL. PTEN represses RNA polymerase III-dependent transcription by targeting the TFIIIB complex. Mol Cell Biol. 2008; 28:4204–14. 10.1128/MCB.01912-07 PubMed DOI PMC
Kantidakis T, Ramsbottom BA, Birch JL, Dowding SN, White RJ. mTOR associates with TFIIIC, is found at tRNA and 5S rRNA genes, and targets their repressor Maf1. Proc Natl Acad Sci USA. 2010; 107:11823–28. 10.1073/pnas.1005188107 PubMed DOI PMC
Zhai W, Comai L. Repression of RNA polymerase I transcription by the tumor suppressor p53. Mol Cell Biol. 2000; 20:5930–38. 10.1128/MCB.20.16.5930-5938.2000 PubMed DOI PMC
Crighton D, Woiwode A, Zhang C, Mandavia N, Morton JP, Warnock LJ, Milner J, White RJ, Johnson DL. p53 represses RNA polymerase III transcription by targeting TBP and inhibiting promoter occupancy by TFIIIB. EMBO J. 2003; 22:2810–20. 10.1093/emboj/cdg265 PubMed DOI PMC
Gartel AL, Tyner AL. Transcriptional regulation of the p21((WAF1/CIP1)) gene. Exp Cell Res. 1999; 246:280–89. 10.1006/excr.1998.4319 PubMed DOI
Harper JW, Elledge SJ, Keyomarsi K, Dynlacht B, Tsai LH, Zhang P, Dobrowolski S, Bai C, Connell-Crowley L, Swindell E. Inhibition of cyclin-dependent kinases by p21. Mol Biol Cell. 1995; 6:387–400. 10.1091/mbc.6.4.387 PubMed DOI PMC
Cavanaugh AH, Hempel WM, Taylor LJ, Rogalsky V, Todorov G, Rothblum LI. Activity of RNA polymerase I transcription factor UBF blocked by Rb gene product. Nature. 1995; 374:177–80. 10.1038/374177a0 PubMed DOI
Hannan KM, Hannan RD, Smith SD, Jefferson LS, Lun M, Rothblum LI. Rb and p130 regulate RNA polymerase I transcription: rb disrupts the interaction between UBF and SL-1. Oncogene. 2000; 19:4988–99. 10.1038/sj.onc.1203875 PubMed DOI
Scott PH, Cairns CA, Sutcliffe JE, Alzuherri HM, McLees A, Winter AG, White RJ. Regulation of RNA polymerase III transcription during cell cycle entry. J Biol Chem. 2001; 276:1005–14. 10.1074/jbc.M005417200 PubMed DOI
Prieto JL, McStay B. Recruitment of factors linking transcription and processing of pre-rRNA to NOR chromatin is UBF-dependent and occurs independent of transcription in human cells. Genes Dev. 2007; 21:2041–54. 10.1101/gad.436707 PubMed DOI PMC
Mullineux ST, Lafontaine DL. Mapping the cleavage sites on mammalian pre-rRNAs: where do we stand? Biochimie. 2012; 94:1521–32. 10.1016/j.biochi.2012.02.001 PubMed DOI
Watkins NJ, Bohnsack MT. The box C/D and H/ACA snoRNPs: key players in the modification, processing and the dynamic folding of ribosomal RNA. Wiley Interdiscip Rev RNA. 2012; 3:397–414. 10.1002/wrna.117 PubMed DOI
Angrisani A, Vicidomini R, Turano M, Furia M. Human dyskerin: beyond telomeres. Biol Chem. 2014; 395:593–610. 10.1515/hsz-2013-0287 PubMed DOI
Cong R, Das S, Ugrinova I, Kumar S, Mongelard F, Wong J, Bouvet P. Interaction of nucleolin with ribosomal RNA genes and its role in RNA polymerase I transcription. Nucleic Acids Res. 2012; 40:9441–54. 10.1093/nar/gks720 PubMed DOI PMC
Angelov D, Bondarenko VA, Almagro S, Menoni H, Mongélard F, Hans F, Mietton F, Studitsky VM, Hamiche A, Dimitrov S, Bouvet P. Nucleolin is a histone chaperone with FACT-like activity and assists remodeling of nucleosomes. EMBO J. 2006; 25:1669–79. 10.1038/sj.emboj.7601046 PubMed DOI PMC
Ginisty H, Amalric F, Bouvet P. Nucleolin functions in the first step of ribosomal RNA processing. EMBO J. 1998; 17:1476–86. 10.1093/emboj/17.5.1476 PubMed DOI PMC
Ginisty H, Serin G, Ghisolfi-Nieto L, Roger B, Libante V, Amalric F, Bouvet P. Interaction of nucleolin with an evolutionarily conserved pre-ribosomal RNA sequence is required for the assembly of the primary processing complex. J Biol Chem. 2000; 275:18845–50. 10.1074/jbc.M002350200 PubMed DOI
Bouvet P, Diaz JJ, Kindbeiter K, Madjar JJ, Amalric F. Nucleolin interacts with several ribosomal proteins through its RGG domain. J Biol Chem. 1998; 273:19025–29. 10.1074/jbc.273.30.19025 PubMed DOI
Roger B, Moisand A, Amalric F, Bouvet P. Nucleolin provides a link between RNA polymerase I transcription and pre-ribosome assembly. Chromosoma. 2003; 111:399–407. 10.1007/s00412-002-0221-5 PubMed DOI
Murano K, Okuwaki M, Hisaoka M, Nagata K. Transcription regulation of the rRNA gene by a multifunctional nucleolar protein, B23/nucleophosmin, through its histone chaperone activity. Mol Cell Biol. 2008; 28:3114–26. 10.1128/MCB.02078-07 PubMed DOI PMC
Savkur RS, Olson MO. Preferential cleavage in pre-ribosomal RNA byprotein B23 endoribonuclease. Nucleic Acids Res. 1998; 26:4508–15. 10.1093/nar/26.19.4508 PubMed DOI PMC
Itahana K, Bhat KP, Jin A, Itahana Y, Hawke D, Kobayashi R, Zhang Y. Tumor suppressor ARF degrades B23, a nucleolar protein involved in ribosome biogenesis and cell proliferation. Mol Cell. 2003; 12:1151–64. 10.1016/S1097-2765(03)00431-3 PubMed DOI
Yu Y, Maggi LB Jr, Brady SN, Apicelli AJ, Dai MS, Lu H, Weber JD. Nucleophosmin is essential for ribosomal protein L5 nuclear export. Mol Cell Biol. 2006; 26:3798–809. 10.1128/MCB.26.10.3798-3809.2006 PubMed DOI PMC
Maggi LB Jr, Kuchenruether M, Dadey DY, Schwope RM, Grisendi S, Townsend RR, Pandolfi PP, Weber JD. Nucleophosmin serves as a rate-limiting nuclear export chaperone for the Mammalian ribosome. Mol Cell Biol. 2008; 28:7050–65. 10.1128/MCB.01548-07 PubMed DOI PMC
Box JK, Paquet N, Adams MN, Boucher D, Bolderson E, O’Byrne KJ, Richard DJ. Nucleophosmin: from structure and function to disease development. BMC Mol Biol. 2016; 17:19. 10.1186/s12867-016-0073-9 PubMed DOI PMC
Warner JR, Mitra G, Schwindinger WF, Studeny M, Fried HM. Saccharomyces cerevisiae coordinates accumulation of yeast ribosomal proteins by modulating mRNA splicing, translational initiation, and protein turnover. Mol Cell Biol. 1985; 5:1512–21. 10.1128/MCB.5.6.1512 PubMed DOI PMC
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. 10.1016/j.cub.2007.03.064 PubMed DOI PMC
Jäkel S, Görlich D. Importin beta, transportin, RanBP5 and RanBP7 mediate nuclear import of ribosomal proteins in mammalian cells. EMBO J. 1998; 17:4491–502. 10.1093/emboj/17.15.4491 PubMed DOI PMC
Plafker SM, Macara IG. Ribosomal protein L12 uses a distinct nuclear import pathway mediated by importin 11. Mol Cell Biol. 2002; 22:1266–75. 10.1128/MCB.22.4.1266-1275.2002 PubMed DOI PMC
Jäkel S, Mingot JM, Schwarzmaier P, Hartmann E, Görlich D. Importins fulfil a dual function as nuclear import receptors and cytoplasmic chaperones for exposed basic domains. EMBO J. 2002; 21:377–86. 10.1093/emboj/21.3.377 PubMed DOI PMC
Zhang J, Harnpicharnchai P, Jakovljevic J, Tang L, Guo Y, Oeffinger M, Rout MP, Hiley SL, Hughes T, Woolford JL Jr. Assembly factors Rpf2 and Rrs1 recruit 5S rRNA and ribosomal proteins rpL5 and rpL11 into nascent ribosomes. Genes Dev. 2007; 21:2580–92. 10.1101/gad.1569307 PubMed DOI PMC
Sloan KE, Bohnsack MT, Watkins NJ. The 5S RNP couples p53 homeostasis to ribosome biogenesis and nucleolar stress. Cell Reports. 2013; 5:237–47. 10.1016/j.celrep.2013.08.049 PubMed DOI PMC
Thomas F, Kutay U. Biogenesis and nuclear export of ribosomal subunits in higher eukaryotes depend on the CRM1 export pathway. J Cell Sci. 2003; 116:2409–19. 10.1242/jcs.00464 PubMed DOI
Henras AK, Soudet J, Gérus M, Lebaron S, Caizergues-Ferrer M, Mougin A, Henry Y. The post-transcriptional steps of eukaryotic ribosome biogenesis. Cell Mol Life Sci. 2008; 65:2334–59. 10.1007/s00018-008-8027-0 PubMed DOI PMC
Jackson RJ, Hellen CU, Pestova TV. The mechanism of eukaryotic translation initiation and principles of its regulation. Nat Rev Mol Cell Biol. 2010; 11:113–27. 10.1038/nrm2838 PubMed DOI PMC
Honda R, Tanaka H, Yasuda H. Oncoprotein MDM2 is a ubiquitin ligase E3 for tumor suppressor p53. FEBS Lett. 1997; 420:25–27. 10.1016/S0014-5793(97)01480-4 PubMed DOI
Michael D, Oren M. The p53-Mdm2 module and the ubiquitin system. Semin Cancer Biol. 2003; 13:49–58. 10.1016/S1044-579X(02)00099-8 PubMed DOI
Haupt Y, Maya R, Kazaz A, Oren M. Mdm2 promotes the rapid degradation of p53. Nature. 1997; 387:296–99. 10.1038/387296a0 PubMed DOI
Gu J, Kawai H, Nie L, Kitao H, Wiederschain D, Jochemsen AG, Parant J, Lozano G, Yuan ZM. Mutual dependence of MDM2 and MDMX in their functional inactivation of p53. J Biol Chem. 2002; 277:19251–54. 10.1074/jbc.C200150200 PubMed DOI
Hock AK, Vousden KH. The role of ubiquitin modification in the regulation of p53. Biochim Biophys Acta. 2014; 1843:137–49. 10.1016/j.bbamcr.2013.05.022 PubMed DOI
Toledo F, Wahl GM. Regulating the p53 pathway: in vitro hypotheses, in vivo veritas. Nat Rev Cancer. 2006; 6:909–23. 10.1038/nrc2012 PubMed DOI
Picksley SM, Lane DP. The p53-mdm2 autoregulatory feedback loop: a paradigm for the regulation of growth control by p53? BioEssays. 1993; 15:689–90. 10.1002/bies.950151008 PubMed DOI
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. 10.1038/nrm2451 PubMed DOI
Zhang Y, Lu H. Signaling to p53: ribosomal proteins find their way. Cancer Cell. 2009; 16:369–77. 10.1016/j.ccr.2009.09.024 PubMed DOI PMC
Fumagalli S, Ivanenkov VV, Teng T, Thomas G. Suprainduction of p53 by disruption of 40S and 60S ribosome biogenesis leads to the activation of a novel G2/M checkpoint. Genes Dev. 2012; 26:1028–40. 10.1101/gad.189951.112 PubMed DOI PMC
Bursać S, Brdovčak MC, Pfannkuchen M, Orsolić I, Golomb L, Zhu Y, Katz C, Daftuar L, Grabušić K, Vukelić I, Filić V, Oren M, Prives C, Volarevic S. Mutual protection of ribosomal proteins L5 and L11 from degradation is essential for p53 activation upon ribosomal biogenesis stress. Proc Natl Acad Sci USA. 2012; 109:20467–72. 10.1073/pnas.1218535109 PubMed DOI PMC
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. 10.1016/0022-2836(77)90157-7 PubMed DOI
Donati G, Peddigari S, Mercer CA, Thomas G. 5S ribosomal RNA is an essential component of a nascent ribosomal precursor complex that regulates the Hdm2-p53 checkpoint. Cell Reports. 2013; 4:87–98. 10.1016/j.celrep.2013.05.045 PubMed DOI PMC
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. 10.1093/emboj/cdg579 PubMed DOI PMC
Fumagalli S, Di Cara A, Neb-Gulati A, Natt F, Schwemberger S, Hall J, Babcock GF, Bernardi R, Pandolfi PP, Thomas G. Absence of nucleolar disruption after impairment of 40S ribosome biogenesis reveals an rpL11-translation-dependent mechanism of p53 induction. Nat Cell Biol. 2009; 11:501–08. 10.1038/ncb1858 PubMed DOI PMC
Bursac S, Brdovcak MC, Donati G, Volarevic S. Activation of the tumor suppressor p53 upon impairment of ribosome biogenesis. Biochim Biophys Acta. 2014; 1842:817–30. 10.1016/j.bbadis.2013.08.014 PubMed DOI
Sherr CJ. Divorcing ARF and p53: an unsettled case. Nat Rev Cancer. 2006; 6:663–73. 10.1038/nrc1954 PubMed DOI
Quelle DE, Zindy F, Ashmun RA, Sherr CJ. Alternative reading frames of the INK4a tumor suppressor gene encode two unrelated proteins capable of inducing cell cycle arrest. Cell. 1995; 83:993–1000. 10.1016/0092-8674(95)90214-7 PubMed DOI
Korgaonkar C, Hagen J, Tompkins V, Frazier AA, Allamargot C, Quelle FW, Quelle DE. Nucleophosmin (B23) targets ARF to nucleoli and inhibits its function. Mol Cell Biol. 2005; 25:1258–71. 10.1128/MCB.25.4.1258-1271.2005 PubMed DOI PMC
Sherr CJ. Ink4-Arf locus in cancer and aging. Wiley Interdiscip Rev Dev Biol. 2012; 1:731–41. 10.1002/wdev.40 PubMed DOI PMC
Midgley CA, Desterro JM, Saville MK, Howard S, Sparks A, Hay RT, Lane DP. An N-terminal p14ARF peptide blocks Mdm2-dependent ubiquitination in vitro and can activate p53 in vivo. Oncogene. 2000; 19:2312–23. 10.1038/sj.onc.1203593 PubMed DOI
Qin FX, Shao HY, Chen XC, Tan S, Zhang HJ, Miao ZY, Wang L, Hui-Chen, Zhang L. Knockdown of NPM1 by RNA interference inhibits cells proliferation and induces apoptosis in leukemic cell line. Int J Med Sci. 2011; 8:287–94. 10.7150/ijms.8.287 PubMed DOI PMC
Lessard F, Morin F, Ivanchuk S, Langlois F, Stefanovsky V, Rutka J, Moss T. The ARF tumor suppressor controls ribosome biogenesis by regulating the RNA polymerase I transcription factor TTF-I. Mol Cell. 2010; 38:539–50. 10.1016/j.molcel.2010.03.015 PubMed DOI
Ayrault O, Andrique L, Fauvin D, Eymin B, Gazzeri S, Séité P. Human tumor suppressor p14ARF negatively regulates rRNA transcription and inhibits UBF1 transcription factor phosphorylation. Oncogene. 2006; 25:7577–86. 10.1038/sj.onc.1209743 PubMed DOI
Kurki S, Peltonen K, Latonen L, Kiviharju TM, Ojala PM, Meek D, Laiho M. Nucleolar protein NPM interacts with HDM2 and protects tumor suppressor protein p53 from HDM2-mediated degradation. Cancer Cell. 2004; 5:465–75. 10.1016/S1535-6108(04)00110-2 PubMed DOI
Dhar SK, St Clair DK. Nucleophosmin blocks mitochondrial localization of p53 and apoptosis. J Biol Chem. 2009; 284:16409–18. 10.1074/jbc.M109.005736 PubMed DOI PMC
Kerr LE, Birse-Archbold JL, Short DM, McGregor AL, Heron I, Macdonald DC, Thompson J, Carlson GJ, Kelly JS, McCulloch J, Sharkey J. Nucleophosmin is a novel Bax chaperone that regulates apoptotic cell death. Oncogene. 2007; 26:2554–62. 10.1038/sj.onc.1210044 PubMed DOI
Donati G, Brighenti E, Vici M, Mazzini G, Treré D, Montanaro L, Derenzini M. Selective inhibition of rRNA transcription downregulates E2F-1: a new p53-independent mechanism linking cell growth to cell proliferation. J Cell Sci. 2011; 124:3017–28. 10.1242/jcs.086074 PubMed DOI
Zhang Z, Wang H, Li M, Rayburn ER, Agrawal S, Zhang R. Stabilization of E2F1 protein by MDM2 through the E2F1 ubiquitination pathway. Oncogene. 2005; 24:7238–47. 10.1038/sj.onc.1208814 PubMed DOI
Crosby ME, Almasan A. Opposing roles of E2Fs in cell proliferation and death. Cancer Biol Ther. 2004; 3:1208–11. 10.4161/cbt.3.12.1494 PubMed DOI PMC
Hollstein M, Sidransky D, Vogelstein B, Harris CC. p53 mutations in human cancers. Science. 1991; 253:49–53. 10.1126/science.1905840 PubMed DOI
Orsolic I, Jurada D, Pullen N, Oren M, Eliopoulos AG, Volarevic S. The relationship between the nucleolus and cancer: current evidence and emerging paradigms. Semin Cancer Biol. 2016; 37-38:36–50. 10.1016/j.semcancer.2015.12.004 PubMed DOI
Holmberg Olausson K, Nistér M, Lindström MS. p53 -Dependent and -Independent Nucleolar Stress Responses. Cells. 2012; 1:774–98. 10.3390/cells1040774 PubMed DOI PMC
Donati G, Bertoni S, Brighenti E, Vici M, Treré D, Volarevic S, Montanaro L, Derenzini M. The balance between rRNA and ribosomal protein synthesis up- and downregulates the tumour suppressor p53 in mammalian cells. Oncogene. 2011; 30:3274–88. 10.1038/onc.2011.48 PubMed DOI
Yuan X, Zhou Y, Casanova E, Chai M, Kiss E, Gröne HJ, Schütz G, Grummt I. 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. 10.1016/j.molcel.2005.05.023 PubMed DOI
Hernandez-Verdun D, Roussel P, Thiry M, Sirri V, Lafontaine DL. The nucleolus: structure/function relationship in RNA metabolism. Wiley Interdiscip Rev RNA. 2010; 1:415–31. 10.1002/wrna.39 PubMed DOI
Burger K, Mühl B, Harasim T, Rohrmoser M, Malamoussi A, Orban M, Kellner M, Gruber-Eber A, Kremmer E, Hölzel M, Eick D. Chemotherapeutic drugs inhibit ribosome biogenesis at various levels. J Biol Chem. 2010; 285:12416–25. 10.1074/jbc.M109.074211 PubMed DOI PMC
Peltonen K, Colis L, Liu H, Jäämaa S, Moore HM, Enbäck J, Laakkonen P, Vaahtokari A, Jones RJ, af Hällström TM, Laiho M. Identification of novel p53 pathway activating small-molecule compounds reveals unexpected similarities with known therapeutic agents. PLoS One. 2010; 5:e12996. 10.1371/journal.pone.0012996 PubMed DOI PMC
Peltonen K, Colis L, Liu H, Trivedi R, Moubarek MS, Moore HM, Bai B, Rudek MA, Bieberich CJ, Laiho M. A targeting modality for destruction of RNA polymerase I that possesses anticancer activity. Cancer Cell. 2014; 25:77–90. 10.1016/j.ccr.2013.12.009 PubMed DOI PMC
Drygin D, Siddiqui-Jain A, O’Brien S, Schwaebe M, Lin A, Bliesath J, Ho CB, Proffitt C, Trent K, Whitten JP, Lim JK, Von Hoff D, Anderes K, Rice WG. Anticancer activity of CX-3543: a direct inhibitor of rRNA biogenesis. Cancer Res. 2009; 69:7653–61. 10.1158/0008-5472.CAN-09-1304 PubMed DOI
Drygin D, Lin A, Bliesath J, Ho CB, O’Brien SE, Proffitt C, Omori M, Haddach M, Schwaebe MK, Siddiqui-Jain A, Streiner N, Quin JE, Sanij E, et al.. Targeting RNA polymerase I with an oral small molecule CX-5461 inhibits ribosomal RNA synthesis and solid tumor growth. Cancer Res. 2011; 71:1418–30. 10.1158/0008-5472.CAN-10-1728 PubMed DOI
Bywater MJ, Poortinga G, Sanij E, Hein N, Peck A, Cullinane C, Wall M, Cluse L, Drygin D, Anderes K, Huser N, Proffitt C, Bliesath J, et al.. Inhibition of RNA polymerase I as a therapeutic strategy to promote cancer-specific activation of p53. Cancer Cell. 2012; 22:51–65. 10.1016/j.ccr.2012.05.019 PubMed DOI PMC
National Health and Medical Research Council. (2013). A Phase 1, Open-Label, Dose Escalation, Safety, Pharmacokinetic, and Pharmacodynamic Study of Intravenously Administered CX-5461 in Patients with Advanced Haematologic Malignancies. https://www.anzctr.org.au/Trial/Registration/TrialReview.aspx?id=364713 Registration number:ACTRN12613001061729. Australian New Zealand Clinical Trials Registry.
Canadian Cancer Trials Group. (2016). A Phase I Study of CX5461. Available from: https://ClinicalTrials.gov/show/NCT02719977. NLM identifier: NCT02719977
Xu H, Di Antonio M, McKinney S, Mathew V, Ho B, O’Neil NJ, Santos ND, Silvester J, Wei V, Garcia J, Kabeer F, Lai D, Soriano P, et al.. CX-5461 is a DNA G-quadruplex stabilizer with selective lethality in BRCA1/2 deficient tumours. Nat Commun. 2017; 8:14432. 10.1038/ncomms14432 PubMed DOI PMC
Onofrillo C. (2013). Ribosome Biogenesis and cell cycle regulation: Effect of RNA Polymerase III inhibition [dissertation]. Oncologia e Patologia Sperimentale: Uniiversiittà dii Bollogna.
Engelke DR, Ng SY, Shastry BS, Roeder RG. Specific interaction of a purified transcription factor with an internal control region of 5S RNA genes. Cell. 1980; 19:717–28. 10.1016/S0092-8674(80)80048-1 PubMed DOI
Shastry BS, Honda BM, Roeder RG. Altered levels of a 5 S gene-specific transcription factor (TFIIIA) during oogenesis and embryonic development of Xenopus laevis. J Biol Chem. 1984; 259:11373–82. PubMed
Nishimura K, Kumazawa T, Kuroda T, Katagiri N, Tsuchiya M, Goto N, Furumai R, Murayama A, Yanagisawa J, Kimura K. Perturbation of ribosome biogenesis drives cells into senescence through 5S RNP-mediated p53 activation. Cell Reports. 2015; 10:1310–23. 10.1016/j.celrep.2015.01.055 PubMed DOI
Chang CC, Steinbacher DM. Treacher collins syndrome. Semin Plast Surg. 2012; 26:83–90. 10.1055/s-0032-1320066 PubMed DOI PMC
Posnick JC. Principles and Practice of Orthognathic Surgery. Elsevier Health Sciences. Chapter 4, Frequently Seen Malformations with Dentofacial Deformity. 2013; p. 1059-94.
Kadakia S, Helman SN, Badhey AK, Saman M, Ducic Y. Treacher Collins Syndrome: the genetics of a craniofacial disease. Int J Pediatr Otorhinolaryngol. 2014; 78:893–98. 10.1016/j.ijporl.2014.03.006 PubMed DOI
Ahmed MK, Ye X, Taub PJ. Review of the Genetic Basis of Jaw Malformations. J Pediatr Genet. 2016; 5:209–19. 10.1055/s-0036-1593505 PubMed DOI PMC
Valdez BC, Henning D, So RB, Dixon J, Dixon MJ. The Treacher Collins syndrome (TCOF1) gene product is involved in ribosomal DNA gene transcription by interacting with upstream binding factor. Proc Natl Acad Sci USA. 2004; 101:10709–14. 10.1073/pnas.0402492101 PubMed DOI PMC
Gonzales B, Henning D, So RB, Dixon J, Dixon MJ, Valdez BC. The Treacher Collins syndrome (TCOF1) gene product is involved in pre-rRNA methylation. Hum Mol Genet. 2005; 14:2035–43. 10.1093/hmg/ddi208 PubMed DOI
Dixon J, Jones NC, Sandell LL, Jayasinghe SM, Crane J, Rey JP, Dixon MJ, Trainor PA. Tcof1/Treacle is required for neural crest cell formation and proliferation deficiencies that cause craniofacial abnormalities. Proc Natl Acad Sci USA. 2006; 103:13403–08. 10.1073/pnas.0603730103 PubMed DOI PMC
Graham A, Koentges G, Lumsden A. Neural Crest Apoptosis and the Establishment of Craniofacial Pattern: An Honorable Death. Mol Cell Neurosci. 1996; 8:76–83. 10.1006/mcne.1996.0046 PubMed DOI
Jones NC, Lynn ML, Gaudenz K, Sakai D, Aoto K, Rey JP, Glynn EF, Ellington L, Du C, Dixon J, Dixon MJ, Trainor PA. Prevention of the neurocristopathy Treacher Collins syndrome through inhibition of p53 function. Nat Med. 2008; 14:125–33. 10.1038/nm1725 PubMed DOI PMC
Larsen DH, Hari F, Clapperton JA, Gwerder M, Gutsche K, Altmeyer M, Jungmichel S, Toledo LI, Fink D, Rask MB, Grøfte M, Lukas C, Nielsen ML, et al.. The NBS1-Treacle complex controls ribosomal RNA transcription in response to DNA damage. Nat Cell Biol. 2014; 16:792–803. 10.1038/ncb3007 PubMed DOI PMC
Ciccia A, Huang JW, Izhar L, Sowa ME, Harper JW, Elledge SJ. Treacher Collins syndrome TCOF1 protein cooperates with NBS1 in the DNA damage response. Proc Natl Acad Sci USA. 2014; 111:18631–36. 10.1073/pnas.1422488112 PubMed DOI PMC
Sakai D, Dixon J, Achilleos A, Dixon M, Trainor PA. Prevention of Treacher Collins syndrome craniofacial anomalies in mouse models via maternal antioxidant supplementation. Nat Commun. 2016; 7:10328. 10.1038/ncomms10328 PubMed DOI PMC
Cadet J, Wagner JR. DNA base damage by reactive oxygen species, oxidizing agents, and UV radiation. Cold Spring Harb Perspect Biol. 2013; 5:a012559. 10.1101/cshperspect.a012559 PubMed DOI PMC
Jena NR. DNA damage by reactive species: Mechanisms, mutation and repair. J Biosci. 2012; 37:503–17. 10.1007/s12038-012-9218-2 PubMed DOI
Calo E, Gu B, Bowen ME, Aryan F, Zalc A, Liang J, Flynn RA, Swigut T, Chang HY, Attardi LD, Wysocka J. Tissue-selective effects of nucleolar stress and rDNA damage in developmental disorders. Nature. 2018; 554:112–17. 10.1038/nature25449 PubMed DOI PMC
Turi Z, Senkyrikova M, Mistrik M, Bartek J, Moudry P. Perturbation of RNA Polymerase I transcription machinery by ablation of HEATR1 triggers the RPL5/RPL11-MDM2-p53 ribosome biogenesis stress checkpoint pathway in human cells. Cell Cycle. 2018; 17:92–101. 10.1080/15384101.2017.1403685 PubMed DOI PMC
Gallagher JE, Dunbar DA, Granneman S, Mitchell BM, Osheim Y, Beyer AL, Baserga SJ. RNA polymerase I transcription and pre-rRNA processing are linked by specific SSU processome components. Genes Dev. 2004; 18:2506–17. 10.1101/gad.1226604 PubMed DOI PMC
Dez C, Dlakić M, Tollervey D. Roles of the HEAT repeat proteins Utp10 and Utp20 in 40S ribosome maturation. RNA. 2007; 13:1516–27. 10.1261/rna.609807 PubMed DOI PMC
Krogan NJ, Peng WT, Cagney G, Robinson MD, Haw R, Zhong G, Guo X, Zhang X, Canadien V, Richards DP, Beattie BK, Lalev A, Zhang W, et al.. High-definition macromolecular composition of yeast RNA-processing complexes. Mol Cell. 2004; 13:225–39. 10.1016/S1097-2765(04)00003-6 PubMed DOI
Shav-Tal Y, Blechman J, Darzacq X, Montagna C, Dye BT, Patton JG, Singer RH, Zipori D. Dynamic sorting of nuclear components into distinct nucleolar caps during transcriptional inhibition. Mol Biol Cell. 2005; 16:2395–413. 10.1091/mbc.e04-11-0992 PubMed DOI PMC
Peng Q, Wu J, Zhang Y, Liu Y, Kong R, Hu L, Du X, Ke Y. 1A6/DRIM, a novel t-UTP, activates RNA polymerase I transcription and promotes cell proliferation. PLoS One. 2010; 5:e14244. 10.1371/journal.pone.0014244 PubMed DOI PMC
Zhao C, Andreeva V, Gibert Y, LaBonty M, Lattanzi V, Prabhudesai S, Zhou Y, Zon L, McCann KL, Baserga S, Yelick PC. Tissue specific roles for the ribosome biogenesis factor Wdr43 in zebrafish development. PLoS Genet. 2014; 10:e1004074. 10.1371/journal.pgen.1004074 PubMed DOI PMC
Griffin JN, Sondalle SB, Del Viso F, Baserga SJ, Khokha MK. The ribosome biogenesis factor Nol11 is required for optimal rDNA transcription and craniofacial development in Xenopus. PLoS Genet. 2015; 11:e1005018. 10.1371/journal.pgen.1005018 PubMed DOI PMC
Hölzel M, Rohrmoser M, Schlee M, Grimm T, Harasim T, Malamoussi A, Gruber-Eber A, Kremmer E, Hiddemann W, Bornkamm GW, Eick D. 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. 10.1083/jcb.200501141 PubMed DOI PMC
Yu W, Qiu Z, Gao N, Wang L, Cui H, Qian Y, Jiang L, Luo J, Yi Z, Lu H, Li D, Liu M. PAK1IP1, a ribosomal stress-induced nucleolar protein, regulates cell proliferation via the p53-MDM2 loop. Nucleic Acids Res. 2011; 39:2234–48. 10.1093/nar/gkq1117 PubMed DOI PMC
McMahon M, Ayllón V, Panov KI, O’Connor R. Ribosomal 18 S RNA processing by the IGF-I-responsive WDR3 protein is integrated with p53 function in cancer cell proliferation. J Biol Chem. 2010; 285:18309–18. 10.1074/jbc.M110.108555 PubMed DOI PMC
Skarie JM, Link BA. The primary open-angle glaucoma gene WDR36 functions in ribosomal RNA processing and interacts with the p53 stress-response pathway. Hum Mol Genet. 2008; 17:2474–85. 10.1093/hmg/ddn147 PubMed DOI PMC
Watanabe-Susaki K, Takada H, Enomoto K, Miwata K, Ishimine H, Intoh A, Ohtaka M, Nakanishi M, Sugino H, Asashima M, Kurisaki A. Biosynthesis of ribosomal RNA in nucleoli regulates pluripotency and differentiation ability of pluripotent stem cells. Stem Cells. 2014; 32:3099–111. 10.1002/stem.1825 PubMed DOI
Langhendries JL, Nicolas E, Doumont G, Goldman S, Lafontaine DL. The human box C/D snoRNAs U3 and U8 are required for pre-rRNA processing and tumorigenesis. Oncotarget. 2016; 7:59519–34. 10.18632/oncotarget.11148 PubMed DOI PMC
Choi YW, Kim YW, Bae SM, Kwak SY, Chun HJ, Tong SY, Lee HN, Shin JC, Kim KT, Kim YJ, Ahn WS. Identification of differentially expressed genes using annealing control primer-based GeneFishing in human squamous cell cervical carcinoma. Clin Oncol (R Coll Radiol). 2007; 19:308–18. 10.1016/j.clon.2007.02.010 PubMed DOI
Koh CM, Gurel B, Sutcliffe S, Aryee MJ, Schultz D, Iwata T, Uemura M, Zeller KI, Anele U, Zheng Q, Hicks JL, Nelson WG, Dang CV, et al.. Alterations in nucleolar structure and gene expression programs in prostatic neoplasia are driven by the MYC oncogene. Am J Pathol. 2011; 178:1824–34. 10.1016/j.ajpath.2010.12.040 PubMed DOI PMC
Su H, Xu T, Ganapathy S, Shadfan M, Long M, Huang TH, Thompson I, Yuan ZM. Elevated snoRNA biogenesis is essential in breast cancer. Oncogene. 2014; 33:1348–58. 10.1038/onc.2013.89 PubMed DOI
Belin S, Beghin A, Solano-Gonzàlez E, Bezin L, Brunet-Manquat S, Textoris J, Prats AC, Mertani HC, Dumontet C, Diaz JJ. Dysregulation of ribosome biogenesis and translational capacity is associated with tumor progression of human breast cancer cells. PLoS One. 2009; 4:e7147. 10.1371/journal.pone.0007147 PubMed DOI PMC
Marcel V, Ghayad SE, Belin S, Therizols G, Morel AP, Solano-Gonzàlez E, Vendrell JA, Hacot S, Mertani HC, Albaret MA, Bourdon JC, Jordan L, Thompson A, et al.. p53 acts as a safeguard of translational control by regulating fibrillarin and rRNA methylation in cancer. Cancer Cell. 2013; 24:318–30. 10.1016/j.ccr.2013.08.013 PubMed DOI PMC
Sharma S, Marchand V, Motorin Y, Lafontaine DL. Identification of sites of 2′-O-methylation vulnerability in human ribosomal RNAs by systematic mapping. Sci Rep. 2017; 7:11490. 10.1038/s41598-017-09734-9 PubMed DOI PMC
Kirwan M, Dokal I. Dyskeratosis congenita: a genetic disorder of many faces. Clin Genet. 2008; 73:103–12. 10.1111/j.1399-0004.2007.00923.x PubMed DOI
Wilson DB, Link DC, Mason PJ, Bessler M. Inherited bone marrow failure syndromes in adolescents and young adults. Ann Med. 2014; 46:353–63. 10.3109/07853890.2014.915579 PubMed DOI PMC
Fok WC, Niero EL, Dege C, Brenner KA, Sturgeon CM, Batista LF. p53 Mediates Failure of Human Definitive Hematopoiesis in Dyskeratosis Congenita. Stem Cell Reports. 2017; 9:409–18. 10.1016/j.stemcr.2017.06.015 PubMed DOI PMC
Carrillo J, González A, Manguán-García C, Pintado-Berninches L, Perona R. p53 pathway activation by telomere attrition in X-DC primary fibroblasts occurs in the absence of ribosome biogenesis failure and as a consequence of DNA damage. Clin Transl Oncol. 2014; 16:529–38. 10.1007/s12094-013-1112-3 PubMed DOI
Mason PJ, Bessler M. The genetics of dyskeratosis congenita. Cancer Genet. 2011; 204:635–45. 10.1016/j.cancergen.2011.11.002 PubMed DOI PMC
Bellodi C, Kopmar N, Ruggero D. Deregulation of oncogene-induced senescence and p53 translational control in X-linked dyskeratosis congenita. EMBO J. 2010; 29:1865–76. 10.1038/emboj.2010.83 PubMed DOI PMC
Yoon A, Peng G, Brandenburger Y, Zollo O, Xu W, Rego E, Ruggero D. Impaired control of IRES-mediated translation in X-linked dyskeratosis congenita. Science. 2006; 312:902–06. 10.1126/science.1123835 PubMed DOI
Liu B, Zhang J, Huang C, Liu H. Dyskerin overexpression in human hepatocellular carcinoma is associated with advanced clinical stage and poor patient prognosis. PLoS One. 2012; 7:e43147. 10.1371/journal.pone.0043147 PubMed DOI PMC
Sieron P, Hader C, Hatina J, Engers R, Wlazlinski A, Müller M, Schulz WA. DKC1 overexpression associated with prostate cancer progression. Br J Cancer. 2009; 101:1410–16. 10.1038/sj.bjc.6605299 PubMed DOI PMC
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. 10.1016/j.cell.2005.07.034 PubMed DOI
Jia W, Yao Z, Zhao J, Guan Q, Gao L. New perspectives of physiological and pathological functions of nucleolin (NCL). Life Sci. 2017; 186:1–10. 10.1016/j.lfs.2017.07.025 PubMed DOI
Abdelmohsen K, Gorospe M. RNA-binding protein nucleolin in disease. RNA Biol. 2012; 9:799–808. 10.4161/rna.19718 PubMed DOI PMC
Berger CM, Gaume X, Bouvet P. The roles of nucleolin subcellular localization in cancer. Biochimie. 2015; 113:78–85. 10.1016/j.biochi.2015.03.023 PubMed DOI
Farin K, Schokoroy S, Haklai R, Cohen-Or I, Elad-Sfadia G, Reyes-Reyes ME, Bates PJ, Cox AD, Kloog Y, Pinkas-Kramarski R. Oncogenic synergism between ErbB1, nucleolin, and mutant Ras. Cancer Res. 2011; 71:2140–51. 10.1158/0008-5472.CAN-10-2887 PubMed DOI
Tajrishi MM, Tuteja R, Tuteja N. Nucleolin: the most abundant multifunctional phosphoprotein of nucleolus. Commun Integr Biol. 2011; 4:267–75. 10.4161/cib.4.3.14884 PubMed DOI PMC
Soundararajan S, Chen W, Spicer EK, Courtenay-Luck N, Fernandes DJ. The nucleolin targeting aptamer AS1411 destabilizes Bcl-2 messenger RNA in human breast cancer cells. Cancer Res. 2008; 68:2358–65. 10.1158/0008-5472.CAN-07-5723 PubMed DOI
Bates PJ, Laber DA, Miller DM, Thomas SD, Trent JO. Discovery and development of the G-rich oligonucleotide AS1411 as a novel treatment for cancer. Exp Mol Pathol. 2009; 86:151–64. 10.1016/j.yexmp.2009.01.004 PubMed DOI PMC
Laber DA, Taft BS, Kloecker GH, Bates PJ, Trent JO, Miller DM. Extended phase I study of AS1411 in renal and non-small cell lung cancers. J Clin Oncol. 2006; 24:13098.
Laber DA, Choudry MA, Taft BS, Bhupalam L, Sharma VR, Hendler FJ, Barnhart KM. A phase I study of AGRO100 in advanced cancer. J Clin Oncol. 2004; 22:3112 10.1200/jco.2004.22.14_suppl.3112 DOI
Rosenberg JE, Bambury RM, Van Allen EM, Drabkin HA, Lara PN Jr, Harzstark AL, Wagle N, Figlin RA, Smith GW, Garraway LA, Choueiri T, Erlandsson F, Laber DA. A phase II trial of AS1411 (a novel nucleolin-targeted DNA aptamer) in metastatic renal cell carcinoma. Invest New Drugs. 2014; 32:178–87. 10.1007/s10637-013-0045-6 PubMed DOI PMC
Stuart RK, Stockerl-Goldstein K, Cooper M, Devetten M, Herzig R, Medeiros B, Schiller G, Wei A, Acton G, Rizzieri D. Randomized phase II trial of the nucleolin targeting aptamer AS1411 combined with high-dose cytarabine in relapsed/refractory acute myeloid leukemia (AML). J Clin Oncol. 2009; 27:7019.
Colombo E, Alcalay M, Pelicci PG. Nucleophosmin and its complex network: a possible therapeutic target in hematological diseases. Oncogene. 2011; 30:2595–609. 10.1038/onc.2010.646 PubMed DOI
Lim MJ, Wang XW. Nucleophosmin and human cancer. Cancer Detect Prev. 2006; 30:481–90. 10.1016/j.cdp.2006.10.008 PubMed DOI PMC
Holmberg Olausson K, Elsir T, Moazemi Goudarzi K, Nistér M, Lindström MS. NPM1 histone chaperone is upregulated in glioblastoma to promote cell survival and maintain nucleolar shape. Sci Rep. 2015; 5:16495. 10.1038/srep16495 PubMed DOI PMC
Coutinho-Camillo CM, Lourenço SV, Nishimoto IN, Kowalski LP, Soares FA. Nucleophosmin, p53, and Ki-67 expression patterns on an oral squamous cell carcinoma tissue microarray. Hum Pathol. 2010; 41:1079–86. 10.1016/j.humpath.2009.12.010 PubMed DOI
Sekhar KR, Benamar M, Venkateswaran A, Sasi S, Penthala NR, Crooks PA, Hann SR, Geng L, Balusu R, Abbas T, Freeman ML. Targeting nucleophosmin 1 represents a rational strategy for radiation sensitization. Int J Radiat Oncol Biol Phys. 2014; 89:1106–14. 10.1016/j.ijrobp.2014.04.012 PubMed DOI PMC
Liu X, Liu D, Qian D, Dai J, An Y, Jiang S, Stanley B, Yang J, Wang B, Liu X, Liu DX. Nucleophosmin (NPM1/B23) interacts with activating transcription factor 5 (ATF5) protein and promotes proteasome- and caspase-dependent ATF5 degradation in hepatocellular carcinoma cells. J Biol Chem. 2012; 287:19599–609. 10.1074/jbc.M112.363622 PubMed DOI PMC
Kim KH, Yoo BC, Kim WK, Hong JP, Kim K, Song EY, Lee JY, Cho JY, Ku JL. CD133 and CD133-regulated nucleophosmin linked to 5-fluorouracil susceptibility in human colon cancer cell line SW620. Electrophoresis. 2014; 35:522–32. 10.1002/elps.201300364 PubMed DOI
Wong JC, Hasan MR, Rahman M, Yu AC, Chan SK, Schaeffer DF, Kennecke HF, Lim HJ, Owen D, Tai IT. Nucleophosmin 1, upregulated in adenomas and cancers of the colon, inhibits p53-mediated cellular senescence. Int J Cancer. 2013; 133:1567–77. 10.1002/ijc.28180 PubMed DOI
Kalra RS, Bapat SA. Enhanced levels of double-strand DNA break repair proteins protect ovarian cancer cells against genotoxic stress-induced apoptosis. J Ovarian Res. 2013; 6:66. 10.1186/1757-2215-6-66 PubMed DOI PMC
Zhou Y, Shen J, Xia L, Wang Y. Estrogen mediated expression of nucleophosmin 1 in human endometrial carcinoma clinical stages through estrogen receptor-α signaling. Cancer Cell Int. 2014; 14:540. 10.1186/s12935-014-0145-1 PubMed DOI PMC
Léotoing L, Meunier L, Manin M, Mauduit C, Decaussin M, Verrijdt G, Claessens F, Benahmed M, Veyssière G, Morel L, Beaudoin C. Influence of nucleophosmin/B23 on DNA binding and transcriptional activity of the androgen receptor in prostate cancer cell. Oncogene. 2008; 27:2858–67. 10.1038/sj.onc.1210942 PubMed DOI
Tsui KH, Cheng AJ, Chang P, Pan TL, Yung BY. Association of nucleophosmin/B23 mRNA expression with clinical outcome in patients with bladder carcinoma. Urology. 2004; 64:839–44. 10.1016/j.urology.2004.05.020 PubMed DOI
Pianta A, Puppin C, Franzoni A, Fabbro D, Di Loreto C, Bulotta S, Deganuto M, Paron I, Tell G, Puxeddu E, Filetti S, Russo D, Damante G. Nucleophosmin is overexpressed in thyroid tumors. Biochem Biophys Res Commun. 2010; 397:499–504. 10.1016/j.bbrc.2010.05.142 PubMed DOI
Leal MF, Mazzotti TK, Calcagno DQ, Cirilo PD, Martinez MC, Demachki S, Assumpção PP, Chammas R, Burbano RR, Smith MC. Deregulated expression of Nucleophosmin 1 in gastric cancer and its clinicopathological implications. BMC Gastroenterol. 2014; 14:9. 10.1186/1471-230X-14-9 PubMed DOI PMC
Karhemo PR, Rivinoja A, Lundin J, Hyvönen M, Chernenko A, Lammi J, Sihto H, Lundin M, Heikkilä P, Joensuu H, Bono P, Laakkonen P. An extensive tumor array analysis supports tumor suppressive role for nucleophosmin in breast cancer. Am J Pathol. 2011; 179:1004–14. 10.1016/j.ajpath.2011.04.009 PubMed DOI PMC
Falini B, Martelli MP, Bolli N, Sportoletti P, Liso A, Tiacci E, Haferlach T. Acute myeloid leukemia with mutated nucleophosmin (NPM1): is it a distinct entity? Blood. 2011; 117:1109–20. 10.1182/blood-2010-08-299990 PubMed DOI
Naoe T, Suzuki T, Kiyoi H, Urano T. Nucleophosmin: a versatile molecule associated with hematological malignancies. Cancer Sci. 2006; 97:963–69. 10.1111/j.1349-7006.2006.00270.x PubMed DOI PMC
Di Matteo A, Franceschini M, Chiarella S, Rocchio S, Travaglini-Allocatelli C, Federici L. Molecules that target nucleophosmin for cancer treatment: an update. Oncotarget. 2016; 7:44821–40. 10.18632/oncotarget.8599 PubMed DOI PMC
Qi W, Shakalya K, Stejskal A, Goldman A, Beeck S, Cooke L, Mahadevan D. NSC348884, a nucleophosmin inhibitor disrupts oligomer formation and induces apoptosis in human cancer cells. Oncogene. 2008; 27:4210–20. 10.1038/onc.2008.54 PubMed DOI
Balusu R, Fiskus W, Rao R, Chong DG, Nalluri S, Mudunuru U, Ma H, Chen L, Venkannagari S, Ha K, Abhyankar S, Williams C, McGuirk J, et al.. Targeting levels or oligomerization of nucleophosmin 1 induces differentiation and loss of survival of human AML cells with mutant NPM1. Blood. 2011; 118:3096–106. 10.1182/blood-2010-09-309674 PubMed DOI PMC
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. 10.1371/journal.pone.0009578 PubMed DOI PMC
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. 10.1128/MCB.24.17.7669-7680.2004 PubMed DOI PMC
Barkić M, Crnomarković S, Grabusić K, Bogetić I, Panić L, Tamarut S, Cokarić M, Jerić I, Vidak S, Volarević S. The p53 tumor suppressor causes congenital malformations in Rpl24-deficient mice and promotes their survival. Mol Cell Biol. 2009; 29:2489–504. 10.1128/MCB.01588-08 PubMed DOI PMC
Sun XX, Wang YG, Xirodimas DP, Dai MS. Perturbation of 60 S ribosomal biogenesis results in ribosomal protein L5- and L11-dependent p53 activation. J Biol Chem. 2010; 285:25812–21. 10.1074/jbc.M109.098442 PubMed DOI PMC
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. 10.4161/cc.9.19.13299 PubMed DOI PMC
Dutt S, Narla A, Lin K, Mullally A, Abayasekara N, Megerdichian C, Wilson FH, Currie T, Khanna-Gupta A, Berliner N, Kutok JL, Ebert BL. Haploinsufficiency for ribosomal protein genes causes selective activation of p53 in human erythroid progenitor cells. Blood. 2011; 117:2567–76. 10.1182/blood-2010-07-295238 PubMed DOI PMC
Zhou X, Hao Q, Liao J, Zhang Q, Lu H. Ribosomal protein S14 unties the MDM2-p53 loop upon ribosomal stress. Oncogene. 2013; 32:388–96. 10.1038/onc.2012.63 PubMed DOI PMC
Daftuar L, Zhu Y, Jacq X, Prives C. Ribosomal proteins RPL37, RPS15 and RPS20 regulate the Mdm2-p53-MdmX network. PLoS One. 2013; 8:e68667. 10.1371/journal.pone.0068667 PubMed DOI PMC
Narla A, Ebert BL. Ribosomopathies: human disorders of ribosome dysfunction. Blood. 2010; 115:3196–205. 10.1182/blood-2009-10-178129 PubMed DOI PMC
Lipton JM, Ellis SR. Diamond-Blackfan anemia: diagnosis, treatment, and molecular pathogenesis. Hematol Oncol Clin North Am. 2009; 23:261–82. 10.1016/j.hoc.2009.01.004 PubMed DOI PMC
Ellis SR, Gleizes PE. Diamond Blackfan anemia: ribosomal proteins going rogue. Semin Hematol. 2011; 48:89–96. 10.1053/j.seminhematol.2011.02.005 PubMed DOI
Nakhoul H, Ke J, Zhou X, Liao W, Zeng SX, Lu H. Ribosomopathies: mechanisms of disease. Clin Med Insights Blood Disord. 2014; 7:7–16. 10.4137/CMBD.S16952 PubMed DOI PMC
Chiabrando D, Tolosano E. Diamond Blackfan Anemia at the Crossroad between Ribosome Biogenesis and Heme Metabolism. Adv Hematol. 2010; 2010:790632. 10.1155/2010/790632 PubMed DOI PMC
Ellis SR. Nucleolar stress in Diamond Blackfan anemia pathophysiology. Biochim Biophys Acta. 2014; 1842:765–68. 10.1016/j.bbadis.2013.12.013 PubMed DOI
Keel SB, Doty RT, Yang Z, Quigley JG, Chen J, Knoblaugh S, Kingsley PD, De Domenico I, Vaughn MB, Kaplan J, Palis J, Abkowitz JL. A heme export protein is required for red blood cell differentiation and iron homeostasis. Science. 2008; 319:825–28. 10.1126/science.1151133 PubMed DOI
McGowan KA, Li JZ, Park CY, Beaudry V, Tabor HK, Sabnis AJ, Zhang W, Fuchs H, de Angelis MH, Myers RM, Attardi LD, Barsh GS. Ribosomal mutations cause p53-mediated dark skin and pleiotropic effects. Nat Genet. 2008; 40:963–70. 10.1038/ng.188 PubMed DOI PMC
Jaako P, Flygare J, Olsson K, Quere R, Ehinger M, Henson A, Ellis S, Schambach A, Baum C, Richter J, Larsson J, Bryder D, Karlsson S. Mice with ribosomal protein S19 deficiency develop bone marrow failure and symptoms like patients with Diamond-Blackfan anemia. Blood. 2011; 118:6087–96. 10.1182/blood-2011-08-371963 PubMed DOI
Danilova N, Sakamoto KM, Lin S. Ribosomal protein S19 deficiency in zebrafish leads to developmental abnormalities and defective erythropoiesis through activation of p53 protein family. Blood. 2008; 112:5228–37. 10.1182/blood-2008-01-132290 PubMed DOI
Torihara H, Uechi T, Chakraborty A, Shinya M, Sakai N, Kenmochi N. Erythropoiesis failure due to RPS19 deficiency is independent of an activated Tp53 response in a zebrafish model of Diamond-Blackfan anaemia. Br J Haematol. 2011; 152:648–54. 10.1111/j.1365-2141.2010.08535.x PubMed DOI
Padron E, Komrokji R, List AF. Biology and treatment of the 5q- syndrome. Expert Rev Hematol. 2011; 4:61–69. 10.1586/ehm.11.2 PubMed DOI
Pellagatti A, Boultwood J. Recent Advances in the 5q- Syndrome. Mediterr J Hematol Infect Dis. 2015; 7:e2015037. 10.4084/mjhid.2015.037 PubMed DOI PMC
Ebert BL, Pretz J, Bosco J, Chang CY, Tamayo P, Galili N, Raza A, Root DE, Attar E, Ellis SR, Golub TR. Identification of RPS14 as a 5q- syndrome gene by RNA interference screen. Nature. 2008; 451:335–39. 10.1038/nature06494 PubMed DOI PMC
Barlow JL, Drynan LF, Hewett DR, Holmes LR, Lorenzo-Abalde S, Lane AL, Jolin HE, Pannell R, Middleton AJ, Wong SH, Warren AJ, Wainscoat JS, Boultwood J, McKenzie AN. A p53-dependent mechanism underlies macrocytic anemia in a mouse model of human 5q- syndrome. Nat Med. 2010; 16:59–66. 10.1038/nm.2063 PubMed DOI PMC
Shi Y, Zhai H, Wang X, Han Z, Liu C, Lan M, Du J, Guo C, Zhang Y, Wu K, Fan D. Ribosomal proteins S13 and L23 promote multidrug resistance in gastric cancer cells by suppressing drug-induced apoptosis. Exp Cell Res. 2004; 296:337–46. 10.1016/j.yexcr.2004.02.009 PubMed DOI
Golomb L, Bublik DR, Wilder S, Nevo R, Kiss V, Grabusic K, Volarevic S, Oren M. Importin 7 and exportin 1 link c-Myc and p53 to regulation of ribosomal biogenesis. Mol Cell. 2012; 45:222–32. 10.1016/j.molcel.2011.11.022 PubMed DOI PMC
Kressler D, Bange G, Ogawa Y, Stjepanovic G, Bradatsch B, Pratte D, Amlacher S, Strauß D, Yoneda Y, Katahira J, Sinning I, Hurt E. Synchronizing nuclear import of ribosomal proteins with ribosome assembly. Science. 2012; 338:666–71. 10.1126/science.1226960 PubMed DOI
Calviño FR, Kharde S, Ori A, Hendricks A, Wild K, Kressler D, Bange G, Hurt E, Beck M, Sinning I. Symportin 1 chaperones 5S RNP assembly during ribosome biogenesis by occupying an essential rRNA-binding site. Nat Commun. 2015; 6:6510. 10.1038/ncomms7510 PubMed DOI PMC
Kazyken D, Kaz Y, Kiyan V, Zhylkibayev AA, Chen CH, Agarwal NK, Sarbassov D. The nuclear import of ribosomal proteins is regulated by mTOR. Oncotarget. 2014; 5:9577–93. 10.18632/oncotarget.2473 PubMed DOI PMC
Finch AJ, Hilcenko C, Basse N, Drynan LF, Goyenechea B, Menne TF, González Fernández A, Simpson P, D’Santos CS, Arends MJ, Donadieu J, Bellanné-Chantelot C, Costanzo M, et al.. Uncoupling of GTP hydrolysis from eIF6 release on the ribosome causes Shwachman-Diamond syndrome. Genes Dev. 2011; 25:917–29. 10.1101/gad.623011 PubMed DOI PMC
Wong CC, Traynor D, Basse N, Kay RR, Warren AJ. Defective ribosome assembly in Shwachman-Diamond syndrome. Blood. 2011; 118:4305–12. 10.1182/blood-2011-06-353938 PubMed DOI
Burwick N, Coats SA, Nakamura T, Shimamura A. Impaired ribosomal subunit association in Shwachman-Diamond syndrome. Blood. 2012; 120:5143–52. 10.1182/blood-2012-04-420166 PubMed DOI PMC
Burroughs L, Woolfrey A, Shimamura A. Shwachman-Diamond syndrome: a review of the clinical presentation, molecular pathogenesis, diagnosis, and treatment. Hematol Oncol Clin North Am. 2009; 23:233–48. 10.1016/j.hoc.2009.01.007 PubMed DOI PMC
Nelson AS, Myers KC. Diagnosis, Treatment, and Molecular Pathology of Shwachman-Diamond Syndrome. Hematol Oncol Clin North Am. 2018; 32:687–700. 10.1016/j.hoc.2018.04.006 PubMed DOI
Austin KM, Leary RJ, Shimamura A. The Shwachman-Diamond SBDS protein localizes to the nucleolus. Blood. 2005; 106:1253–58. 10.1182/blood-2005-02-0807 PubMed DOI PMC
Ganapathi KA, Austin KM, Lee CS, Dias A, Malsch MM, Reed R, Shimamura A. The human Shwachman-Diamond syndrome protein, SBDS, associates with ribosomal RNA. Blood. 2007; 110:1458–65. 10.1182/blood-2007-02-075184 PubMed DOI PMC
Elghetany MT, Alter BP. p53 protein overexpression in bone marrow biopsies of patients with Shwachman-Diamond syndrome has a prevalence similar to that of patients with refractory anemia. Arch Pathol Lab Med. 2002; 126:452–55. PubMed
Dror Y. P53 protein overexpression in Shwachman-Diamond syndrome. Arch Pathol Lab Med. 2002; 126:1157–58. PubMed
Provost E, Wehner KA, Zhong X, Ashar F, Nguyen E, Green R, Parsons MJ, Leach SD. Ribosomal biogenesis genes play an essential and p53-independent role in zebrafish pancreas development. Development. 2012; 139:3232–41. 10.1242/dev.077107 PubMed DOI PMC
Tourlakis ME, Zhang S, Ball HL, Gandhi R, Liu H, Zhong J, Yuan JS, Guidos CJ, Durie PR, Rommens JM. In Vivo Senescence in the Sbds-Deficient Murine Pancreas: Cell-Type Specific Consequences of Translation Insufficiency. PLoS Genet. 2015; 11:e1005288. 10.1371/journal.pgen.1005288 PubMed DOI PMC
Evans DS, Kapahi P, Hsueh WC, Kockel L. TOR signaling never gets old: aging, longevity and TORC1 activity. Ageing Res Rev. 2011; 10:225–37. 10.1016/j.arr.2010.04.001 PubMed DOI PMC
Steffen KK, MacKay VL, Kerr EO, Tsuchiya M, Hu D, Fox LA, Dang N, Johnston ED, Oakes JA, Tchao BN, Pak DN, Fields S, Kennedy BK, Kaeberlein M. Yeast life span extension by depletion of 60s ribosomal subunits is mediated by Gcn4. Cell. 2008; 133:292–302. 10.1016/j.cell.2008.02.037 PubMed DOI PMC
Hansen M, Taubert S, Crawford D, Libina N, Lee SJ, Kenyon C. Lifespan extension by conditions that inhibit translation in Caenorhabditis elegans. Aging Cell. 2007; 6:95–110. 10.1111/j.1474-9726.2006.00267.x PubMed DOI
Chen D, Pan KZ, Palter JE, Kapahi P. Longevity determined by developmental arrest genes in Caenorhabditis elegans. Aging Cell. 2007; 6:525–33. 10.1111/j.1474-9726.2007.00305.x PubMed DOI PMC
Chiocchetti A, Zhou J, Zhu H, Karl T, Haubenreisser O, Rinnerthaler M, Heeren G, Oender K, Bauer J, Hintner H, Breitenbach M, Breitenbach-Koller L. Ribosomal proteins Rpl10 and Rps6 are potent regulators of yeast replicative life span. Exp Gerontol. 2007; 42:275–86. 10.1016/j.exger.2006.11.002 PubMed DOI
Curran SP, Ruvkun G. Lifespan regulation by evolutionarily conserved genes essential for viability. PLoS Genet. 2007; 3:e56. 10.1371/journal.pgen.0030056 PubMed DOI PMC
Kaeberlein M, Powers RW 3rd, Steffen KK, Westman EA, Hu D, Dang N, Kerr EO, Kirkland KT, Fields S, Kennedy BK. Regulation of yeast replicative life span by TOR and Sch9 in response to nutrients. Science. 2005; 310:1193–96. 10.1126/science.1115535 PubMed DOI
Powers RW 3rd, Kaeberlein M, Caldwell SD, Kennedy BK, Fields S. Extension of chronological life span in yeast by decreased TOR pathway signaling. Genes Dev. 2006; 20:174–84. 10.1101/gad.1381406 PubMed DOI PMC
Kapahi P, Zid BM, Harper T, Koslover D, Sapin V, Benzer S. Regulation of lifespan in Drosophila by modulation of genes in the TOR signaling pathway. Curr Biol. 2004; 14:885–90. 10.1016/j.cub.2004.03.059 PubMed DOI PMC
Harrison DE, Strong R, Sharp ZD, Nelson JF, Astle CM, Flurkey K, Nadon NL, Wilkinson JE, Frenkel K, Carter CS, Pahor M, Javors MA, Fernandez E, Miller RA. Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature. 2009; 460:392–95. 10.1038/nature08221 PubMed DOI PMC
Passtoors WM, Beekman M, Deelen J, van der Breggen R, Maier AB, Guigas B, Derhovanessian E, van Heemst D, de Craen AJ, Gunn DA, Pawelec G, Slagboom PE. Gene expression analysis of mTOR pathway: association with human longevity. Aging Cell. 2013; 12:24–31. 10.1111/acel.12015 PubMed DOI
Miller RA, Harrison DE, Astle CM, Baur JA, Boyd AR, de Cabo R, Fernandez E, Flurkey K, Javors MA, Nelson JF, Orihuela CJ, Pletcher S, Sharp ZD, et al.. Rapamycin, but not resveratrol or simvastatin, extends life span of genetically heterogeneous mice. J Gerontol A Biol Sci Med Sci. 2011; 66:191–201. 10.1093/gerona/glq178 PubMed DOI PMC
Hofmann JW, Zhao X, De Cecco M, Peterson AL, Pagliaroli L, Manivannan J, Hubbard GB, Ikeno Y, Zhang Y, Feng B, Li X, Serre T, Qi W, et al.. Reduced expression of MYC increases longevity and enhances healthspan. Cell. 2015; 160:477–88. 10.1016/j.cell.2014.12.016 PubMed DOI PMC
Schosserer M, Minois N, Angerer TB, Amring M, Dellago H, Harreither E, Calle-Perez A, Pircher A, Gerstl MP, Pfeifenberger S, Brandl C, Sonntagbauer M, Kriegner A, et al.. Methylation of ribosomal RNA by NSUN5 is a conserved mechanism modulating organismal lifespan. Nat Commun. 2015; 6:6158. 10.1038/ncomms7158 PubMed DOI PMC
Bemiller PM, Lee LH. Nucleolar changes in senescing WI-38 cells. Mech Ageing Dev. 1978; 8:417–27. 10.1016/0047-6374(78)90041-6 PubMed DOI
Buchwalter A, Hetzer MW. Nucleolar expansion and elevated protein translation in premature aging. Nat Commun. 2017; 8:328. 10.1038/s41467-017-00322-z PubMed DOI PMC
Ruggero D, Pandolfi PP. Does the ribosome translate cancer? Nat Rev Cancer. 2003; 3:179–92. 10.1038/nrc1015 PubMed DOI
Tiku V, Antebi A. Nucleolar Function in Lifespan Regulation. Trends Cell Biol. 2018; 28:662–72. 10.1016/j.tcb.2018.03.007 PubMed DOI
Syntichaki P, Troulinaki K, Tavernarakis N. Protein synthesis is a novel determinant of aging in Caenorhabditis elegans. Ann N Y Acad Sci. 2007; 1119:289–95. 10.1196/annals.1404.001 PubMed DOI
Syntichaki P, Troulinaki K, Tavernarakis N. eIF4E function in somatic cells modulates ageing in Caenorhabditis elegans. Nature. 2007; 445:922–26. 10.1038/nature05603 PubMed DOI
Kaushik S, Cuervo AM. Proteostasis and aging. Nat Med. 2015; 21:1406–15. 10.1038/nm.4001 PubMed DOI
Pan KZ, Palter JE, Rogers AN, Olsen A, Chen D, Lithgow GJ, Kapahi P. Inhibition of mRNA translation extends lifespan in Caenorhabditis elegans. Aging Cell. 2007; 6:111–19. 10.1111/j.1474-9726.2006.00266.x PubMed DOI PMC
López-Otín C, Blasco MA, Partridge L, Serrano M, Kroemer G. The hallmarks of aging. Cell. 2013; 153:1194–217. 10.1016/j.cell.2013.05.039 PubMed DOI PMC
McCay C, Crowell M, Maynard LA. The effect of retarded growth upon the length of life span and upon the ultimate body size. J Nutr. 1935; 10:63–79. 10.1093/jn/10.1.63 PubMed DOI
Al-Regaiey KA. The effects of calorie restriction on aging: a brief review. Eur Rev Med Pharmacol Sci. 2016; 20:2468–73. PubMed
Heilbronn LK, Ravussin E. Calorie restriction and aging: review of the literature and implications for studies in humans. Am J Clin Nutr. 2003; 78:361–69. 10.1093/ajcn/78.3.361 PubMed DOI
Tiku V, Jain C, Raz Y, Nakamura S, Heestand B, Liu W, Späth M, Suchiman HE, Müller RU, Slagboom PE, Partridge L, Antebi A. Small nucleoli are a cellular hallmark of longevity. Nat Commun. 2017; 8:16083. 10.1038/ncomms16083 PubMed DOI PMC
Jack CV, Cruz C, Hull RM, Keller MA, Ralser M, Houseley J. Regulation of ribosomal DNA amplification by the TOR pathway. Proc Natl Acad Sci USA. 2015; 112:9674–79. 10.1073/pnas.1505015112 PubMed DOI PMC
Murayama A, Ohmori K, Fujimura A, Minami H, Yasuzawa-Tanaka K, Kuroda T, Oie S, Daitoku H, Okuwaki M, Nagata K, Fukamizu A, Kimura K, Shimizu T, Yanagisawa J. Epigenetic control of rDNA loci in response to intracellular energy status. Cell. 2008; 133:627–39. 10.1016/j.cell.2008.03.030 PubMed DOI
Cohen HY, Miller C, Bitterman KJ, Wall NR, Hekking B, Kessler B, Howitz KT, Gorospe M, de Cabo R, Sinclair DA. Calorie restriction promotes mammalian cell survival by inducing the SIRT1 deacetylase. Science. 2004; 305:390–92. 10.1126/science.1099196 PubMed DOI
Nemoto S, Fergusson MM, Finkel T. Nutrient availability regulates SIRT1 through a forkhead-dependent pathway. Science. 2004; 306:2105–08. 10.1126/science.1101731 PubMed DOI
Satoh A, Brace CS, Rensing N, Cliften P, Wozniak DF, Herzog ED, Yamada KA, Imai S. Sirt1 extends life span and delays aging in mice through the regulation of Nk2 homeobox 1 in the DMH and LH. Cell Metab. 2013; 18:416–30. 10.1016/j.cmet.2013.07.013 PubMed DOI PMC
Matheu A, Maraver A, Klatt P, Flores I, Garcia-Cao I, Borras C, Flores JM, Viña J, Blasco MA, Serrano M. Delayed ageing through damage protection by the Arf/p53 pathway. Nature. 2007; 448:375–79. 10.1038/nature05949 PubMed DOI
Hulbert AJ, Pamplona R, Buffenstein R, Buttemer WA. Life and death: metabolic rate, membrane composition, and life span of animals. Physiol Rev. 2007; 87:1175–213. 10.1152/physrev.00047.2006 PubMed DOI
Takeuchi Y, Horiuchi T, Kobayashi T. Transcription-dependent recombination and the role of fork collision in yeast rDNA. Genes Dev. 2003; 17:1497–506. 10.1101/gad.1085403 PubMed DOI PMC
Ginno PA, Lott PL, Christensen HC, Korf I, Chédin F. R-loop formation is a distinctive characteristic of unmethylated human CpG island promoters. Mol Cell. 2012; 45:814–25. 10.1016/j.molcel.2012.01.017 PubMed DOI PMC
Helmrich A, Ballarino M, Tora L. Collisions between replication and transcription complexes cause common fragile site instability at the longest human genes. Mol Cell. 2011; 44:966–77. 10.1016/j.molcel.2011.10.013 PubMed DOI
El Hage A, French SL, Beyer AL, Tollervey D. Loss of Topoisomerase I leads to R-loop-mediated transcriptional blocks during ribosomal RNA synthesis. Genes Dev. 2010; 24:1546–58. 10.1101/gad.573310 PubMed DOI PMC
Wahba L, Costantino L, Tan FJ, Zimmer A, Koshland D. S1-DRIP-seq identifies high expression and polyA tracts as major contributors to R-loop formation. Genes Dev. 2016; 30:1327–38. 10.1101/gad.280834.116 PubMed DOI PMC
Vijg J, Suh Y. Genome instability and aging. Annu Rev Physiol. 2013; 75:645–68. 10.1146/annurev-physiol-030212-183715 PubMed DOI
Flach J, Bakker ST, Mohrin M, Conroy PC, Pietras EM, Reynaud D, Alvarez S, Diolaiti ME, Ugarte F, Forsberg EC, Le Beau MM, Stohr BA, Méndez J, et al.. Replication stress is a potent driver of functional decline in ageing haematopoietic stem cells. Nature. 2014; 512:198–202. 10.1038/nature13619 PubMed DOI PMC
Schawalder J, Paric E, Neff NF. Telomere and ribosomal DNA repeats are chromosomal targets of the bloom syndrome DNA helicase. BMC Cell Biol. 2003; 4:15. 10.1186/1471-2121-4-15 PubMed DOI PMC
Sinclair DA, Mills K, Guarente L. Accelerated aging and nucleolar fragmentation in yeast sgs1 mutants. Science. 1997; 277:1313–16. 10.1126/science.277.5330.1313 PubMed DOI
Sinclair DA, Guarente L. Extrachromosomal rDNA circles--a cause of aging in yeast. Cell. 1997; 91:1033–42. 10.1016/S0092-8674(00)80493-6 PubMed DOI
Grierson PM, Lillard K, Behbehani GK, Combs KA, Bhattacharyya S, Acharya S, Groden J. BLM helicase facilitates RNA polymerase I-mediated ribosomal RNA transcription. Hum Mol Genet. 2012; 21:1172–83. 10.1093/hmg/ddr545 PubMed DOI PMC
Shiratori M, Suzuki T, Itoh C, Goto M, Furuichi Y, Matsumoto T. WRN helicase accelerates the transcription of ribosomal RNA as a component of an RNA polymerase I-associated complex. Oncogene. 2002; 21:2447–54. 10.1038/sj.onc.1205334 PubMed DOI
D’Aquila P, Montesanto A, Mandalà M, Garasto S, Mari V, Corsonello A, Bellizzi D, Passarino G. Methylation of the ribosomal RNA gene promoter is associated with aging and age-related decline. Aging Cell. 2017; 16:966–75. 10.1111/acel.12603 PubMed DOI PMC
Jung M, Jin SG, Zhang X, Xiong W, Gogoshin G, Rodin AS, Pfeifer GP. Longitudinal epigenetic and gene expression profiles analyzed by three-component analysis reveal down-regulation of genes involved in protein translation in human aging. Nucleic Acids Res. 2015; 43:e100. 10.1093/nar/gkv473 PubMed DOI PMC
Zhang W, Hawse J, Huang Q, Sheets N, Miller KM, Horwitz J, Kantorow M. Decreased expression of ribosomal proteins in human age-related cataract. Invest Ophthalmol Vis Sci. 2002; 43:198–204. PubMed PMC
Kirby TJ, Lee JD, England JH, Chaillou T, Esser KA, McCarthy JJ. Blunted hypertrophic response in aged skeletal muscle is associated with decreased ribosome biogenesis. J Appl Physiol (1985). 2015; 119:321–27. 10.1152/japplphysiol.00296.2015 PubMed DOI PMC
Barna M, Pusic A, Zollo O, Costa M, Kondrashov N, Rego E, Rao PH, Ruggero D. Suppression of Myc oncogenic activity by ribosomal protein haploinsufficiency. Nature. 2008; 456:971–75. 10.1038/nature07449 PubMed DOI PMC
Ruggero D. Translational control in cancer etiology. Cold Spring Harb Perspect Biol. 2013; 5:5. 10.1101/cshperspect.a012336 PubMed DOI PMC
Xue S, Barna M. Specialized ribosomes: a new frontier in gene regulation and organismal biology. Nat Rev Mol Cell Biol. 2012; 13:355–69. 10.1038/nrm3359 PubMed DOI PMC
Duncan FE, Jasti S, Paulson A, Kelsh JM, Fegley B, Gerton JL. Age-associated dysregulation of protein metabolism in the mammalian oocyte. Aging Cell. 2017; 16:1381–93. 10.1111/acel.12676 PubMed DOI PMC
Guo X, Shi Y, Gou Y, Li J, Han S, Zhang Y, Huo J, Ning X, Sun L, Chen Y, Sun S, Fan D. Human ribosomal protein S13 promotes gastric cancer growth through down-regulating p27(Kip1). J Cell Mol Med. 2011; 15:296–306. 10.1111/j.1582-4934.2009.00969.x PubMed DOI PMC
Du J, Shi Y, Pan Y, Jin X, Liu C, Liu N, Han Q, Lu Y, Qiao T, Fan D. Regulation of multidrug resistance by ribosomal protein l6 in gastric cancer cells. Cancer Biol Ther. 2005; 4:242–47. 10.4161/cbt.4.2.1477 PubMed DOI
Qu J, Bishop JM. Nucleostemin maintains self-renewal of embryonic stem cells and promotes reprogramming of somatic cells to pluripotency. J Cell Biol. 2012; 197:731–45. 10.1083/jcb.201103071 PubMed DOI PMC
Le Bouteiller M, Souilhol C, Beck-Cormier S, Stedman A, Burlen-Defranoux O, Vandormael-Pournin S, Bernex F, Cumano A, Cohen-Tannoudji M. Notchless-dependent ribosome synthesis is required for the maintenance of adult hematopoietic stem cells. J Exp Med. 2013; 210:2351–69. 10.1084/jem.20122019 PubMed DOI PMC
Yang A, Shi G, Zhou C, Lu R, Li H, Sun L, Jin Y. Nucleolin maintains embryonic stem cell self-renewal by suppression of p53 protein-dependent pathway. J Biol Chem. 2011; 286:43370–82. 10.1074/jbc.M111.225185 PubMed DOI PMC
Meshorer E, Misteli T. Chromatin in pluripotent embryonic stem cells and differentiation. Nat Rev Mol Cell Biol. 2006; 7:540–46. 10.1038/nrm1938 PubMed DOI
Hayashi Y, Kuroda T, Kishimoto H, Wang C, Iwama A, Kimura K. Downregulation of rRNA transcription triggers cell differentiation. PLoS One. 2014; 9:e98586. 10.1371/journal.pone.0098586 PubMed DOI PMC
Stedman A, Beck-Cormier S, Le Bouteiller M, Raveux A, Vandormael-Pournin S, Coqueran S, Lejour V, Jarzebowski L, Toledo F, Robine S, Cohen-Tannoudji M. Ribosome biogenesis dysfunction leads to p53-mediated apoptosis and goblet cell differentiation of mouse intestinal stem/progenitor cells. Cell Death Differ. 2015; 22:1865–76. 10.1038/cdd.2015.57 PubMed DOI PMC
Tyner SD, Venkatachalam S, Choi J, Jones S, Ghebranious N, Igelmann H, Lu X, Soron G, Cooper B, Brayton C, Park SH, Thompson T, Karsenty G, et al.. p53 mutant mice that display early ageing-associated phenotypes. Nature. 2002; 415:45–53. 10.1038/415045a PubMed DOI
Maier B, Gluba W, Bernier B, Turner T, Mohammad K, Guise T, Sutherland A, Thorner M, Scrable H. Modulation of mammalian life span by the short isoform of p53. Genes Dev. 2004; 18:306–19. 10.1101/gad.1162404 PubMed DOI PMC
van Heemst D, Mooijaart SP, Beekman M, Schreuder J, de Craen AJ, Brandt BW, Slagboom PE, Westendorp RG, and Long Life study group. Variation in the human TP53 gene affects old age survival and cancer mortality. Exp Gerontol. 2005; 40:11–15. 10.1016/j.exger.2004.10.001 PubMed DOI
Steffen KK, Dillin A. A Ribosomal Perspective on Proteostasis and Aging. Cell Metab. 2016; 23:1004–12. 10.1016/j.cmet.2016.05.013 PubMed DOI
Gomes C, Smith SC, Youssef MN, Zheng JJ, Hagg T, Hetman M. RNA polymerase 1-driven transcription as a mediator of BDNF-induced neurite outgrowth. J Biol Chem. 2011; 286:4357–63. 10.1074/jbc.M110.170134 PubMed DOI PMC
Slomnicki LP, Pietrzak M, Vashishta A, Jones J, Lynch N, Elliot S, Poulos E, Malicote D, Morris BE, Hallgren J, Hetman M. Requirement of Neuronal Ribosome Synthesis for Growth and Maintenance of the Dendritic Tree. J Biol Chem. 2016; 291:5721–39. 10.1074/jbc.M115.682161 PubMed DOI PMC
Kinderman NB, Harrington CA, Drengler SM, Jones KJ. Ribosomal RNA transcriptional activation and processing in hamster facial motoneurons: effects of axotomy with or without exposure to testosterone. J Comp Neurol. 1998; 401:205–16. 10.1002/(SICI)1096-9861(19981116)401:2<205::AID-CNE4>3.0.CO;2-4 PubMed DOI
Storer PD, Jones KJ. Ribosomal RNA transcriptional activation and processing in hamster rubrospinal motoneurons: effects of axotomy and testosterone treatment. J Comp Neurol. 2003; 458:326–33. 10.1002/cne.10623 PubMed DOI
Ding Q, Markesbery WR, Chen Q, Li F, Keller JN. Ribosome dysfunction is an early event in Alzheimer’s disease. J Neurosci. 2005; 25:9171–75. 10.1523/JNEUROSCI.3040-05.2005 PubMed DOI PMC
Honda K, Smith MA, Zhu X, Baus D, Merrick WC, Tartakoff AM, Hattier T, Harris PL, Siedlak SL, Fujioka H, Liu Q, Moreira PI, Miller FP, et al.. Ribosomal RNA in Alzheimer disease is oxidized by bound redox-active iron. J Biol Chem. 2005; 280:20978–86. 10.1074/jbc.M500526200 PubMed DOI
Ding Q, Markesbery WR, Cecarini V, Keller JN. Decreased RNA, and increased RNA oxidation, in ribosomes from early Alzheimer’s disease. Neurochem Res. 2006; 31:705–10. 10.1007/s11064-006-9071-5 PubMed DOI
Pietrzak M, Rempala G, Nelson PT, Zheng JJ, Hetman M. Epigenetic silencing of nucleolar rRNA genes in Alzheimer’s disease. PLoS One. 2011; 6:e22585. 10.1371/journal.pone.0022585 PubMed DOI PMC
Zeng J, Libien J, Shaik F, Wolk J, Hernández AI. Nucleolar PARP-1 Expression Is Decreased in Alzheimer’s Disease: Consequences for Epigenetic Regulation of rDNA and Cognition. Neural Plast. 2016; 2016:8987928. 10.1155/2016/8987928 PubMed DOI PMC
Dönmez-Altuntaş H, Akalin H, Karaman Y, Demirtaş H, Imamoğlu N, Özkul Y. Evaluation of the nucleolar organizer regions in Alzheimer’s disease. Gerontology. 2005; 51:297–301. 10.1159/000086365 PubMed DOI
Bou Samra E, Buhagiar-Labarchède G, Machon C, Guitton J, Onclercq-Delic R, Green MR, Alibert O, Gazin C, Veaute X, Amor-Guéret M. A role for Tau protein in maintaining ribosomal DNA stability and cytidine deaminase-deficient cell survival. Nat Commun. 2017; 8:693. 10.1038/s41467-017-00633-1 PubMed DOI PMC
Sjöberg MK, Shestakova E, Mansuroglu Z, Maccioni RB, Bonnefoy E. Tau protein binds to pericentromeric DNA: a putative role for nuclear tau in nucleolar organization. J Cell Sci. 2006; 119:2025–34. 10.1242/jcs.02907 PubMed DOI
Vanderweyde T, Apicco DJ, Youmans-Kidder K, Ash PE, Cook C, Lummertz da Rocha E, Jansen-West K, Frame AA, Citro A, Leszyk JD, Ivanov P, Abisambra JF, Steffen M, et al.. Interaction of tau with the RNA-Binding Protein TIA1 Regulates tau Pathophysiology and Toxicity. Cell Reports. 2016; 15:1455–66. 10.1016/j.celrep.2016.04.045 PubMed DOI PMC
Maina MB, Bailey LJ, Wagih S, Biasetti L, Pollack SJ, Quinn JP, Thorpe JR, Doherty AJ, Serpell LC. The involvement of tau in nucleolar transcription and the stress response. Acta Neuropathol Commun. 2018; 6:70. 10.1186/s40478-018-0565-6 PubMed DOI PMC
Rieker C, Engblom D, Kreiner G, Domanskyi A, Schober A, Stotz S, Neumann M, Yuan X, Grummt I, Schütz G, Parlato R. Nucleolar disruption in dopaminergic neurons leads to oxidative damage and parkinsonism through repression of mammalian target of rapamycin signaling. J Neurosci. 2011; 31:453–60. 10.1523/JNEUROSCI.0590-10.2011 PubMed DOI PMC
Healy-Stoffel M, Ahmad SO, Stanford JA, Levant B. Altered nucleolar morphology in substantia nigra dopamine neurons following 6-hydroxydopamine lesion in rats. Neurosci Lett. 2013; 546:26–30. 10.1016/j.neulet.2013.04.033 PubMed DOI PMC
Caudle WM, Kitsou E, Li J, Bradner J, Zhang J. A role for a novel protein, nucleolin, in Parkinson’s disease. Neurosci Lett. 2009; 459:11–15. 10.1016/j.neulet.2009.04.060 PubMed DOI PMC
Jin J, Li GJ, Davis J, Zhu D, Wang Y, Pan C, Zhang J. Identification of novel proteins associated with both α-synuclein and DJ-1. Mol Cell Proteomics. 2007; 6:845–59. 10.1074/mcp.M600182-MCP200 PubMed DOI
Vilotti S, Codrich M, Dal Ferro M, Pinto M, Ferrer I, Collavin L, Gustincich S, Zucchelli S. Parkinson’s disease DJ-1 L166P alters rRNA biogenesis by exclusion of TTRAP from the nucleolus and sequestration into cytoplasmic aggregates via TRAF6. PLoS One. 2012; 7:e35051. 10.1371/journal.pone.0035051 PubMed DOI PMC
Kang H, Shin JH. Repression of rRNA transcription by PARIS contributes to Parkinson’s disease. Neurobiol Dis. 2015; 73:220–28. 10.1016/j.nbd.2014.10.003 PubMed DOI
Lee J, Hwang YJ, Boo JH, Han D, Kwon OK, Todorova K, Kowall NW, Kim Y, Ryu H. Dysregulation of upstream binding factor-1 acetylation at K352 is linked to impaired ribosomal DNA transcription in Huntington’s disease. Cell Death Differ. 2011; 18:1726–35. 10.1038/cdd.2011.38 PubMed DOI PMC
Lee J, Hwang YJ, Ryu H, Kowall NW, Ryu H. Nucleolar dysfunction in Huntington’s disease. Biochim Biophys Acta. 2014; 1842:785–90. 10.1016/j.bbadis.2013.09.017 PubMed DOI PMC
Tsoi H, Lau TC, Tsang SY, Lau KF, Chan HY. CAG expansion induces nucleolar stress in polyglutamine diseases. Proc Natl Acad Sci USA. 2012; 109:13428–33. 10.1073/pnas.1204089109 PubMed DOI PMC
Bae BI, Xu H, Igarashi S, Fujimuro M, Agrawal N, Taya Y, Hayward SD, Moran TH, Montell C, Ross CA, Snyder SH, Sawa A. p53 mediates cellular dysfunction and behavioral abnormalities in Huntington’s disease. Neuron. 2005; 47:29–41. 10.1016/j.neuron.2005.06.005 PubMed DOI
Kitamura Y, Shimohama S, Kamoshima W, Matsuoka Y, Nomura Y, Taniguchi T. Changes of p53 in the brains of patients with Alzheimer’s disease. Biochem Biophys Res Commun. 1997; 232:418–21. 10.1006/bbrc.1997.6301 PubMed DOI
Nair VD, McNaught KS, González-Maeso J, Sealfon SC, Olanow CW. p53 mediates nontranscriptional cell death in dopaminergic cells in response to proteasome inhibition. J Biol Chem. 2006; 281:39550–60. 10.1074/jbc.M603950200 PubMed DOI
Boulon S, Westman BJ, Hutten S, Boisvert FM, Lamond AI. The nucleolus under stress. Mol Cell. 2010; 40:216–27. 10.1016/j.molcel.2010.09.024 PubMed DOI PMC