The p53 Tumor Suppressor Causes Congenital Malformations in Rpl24-Deficient Mice and Promotes Their Survival

REFERENCES

• Amsterdam, A., K. C. Sadler, K. Lai, S. Farrington, R. T. Bronson, J. A. Lees, and N. Hopkins. 2004. Many ribosomal protein genes are cancer genes in zebrafish. PLoS Biol. 2:E139.
   PubMed Web of Science ®Google Scholar
• Armstrong, J. F., M. H. Kaufman, D. J. Harrison, and A. R. Clarke. 1995. High-frequency developmental abnormalities in p53-deficient mice. Curr. Biol. 5:931–936.
   PubMed Web of Science ®Google Scholar
• Bhat, K. P., K. Itahana, A. Jin, and Y. Zhang. 2004. Essential role of ribosomal protein L11 in mediating growth inhibition-induced p53 activation. EMBO J. 23:2402–2412.
   PubMed Web of Science ®Google Scholar
• Brugarolas, J., C. Chandrasekaran, J. I. Gordon, D. Beach, T. Jacks, and G. J. Hannon. 1995. Radiation-induced cell cycle arrest compromised by p21 deficiency. Nature 377:552–557.
   PubMed Web of Science ®Google Scholar
• Budanov, A. V., and M. Karin. 2008. p53 target genes sestrin1 and sestrin2 connect genotoxic stress and mTOR signaling. Cell 134:451–460.
   PubMed Web of Science ®Google Scholar
• Budde, A., and I. Grummt. 1999. p53 represses ribosomal gene transcription. Oncogene 18:1119–1124.
   PubMedGoogle Scholar
• Cmejla, R., J. Cmejlova, H. Handrkova, J. Petrak, and D. Pospisilova. 2007. Ribosomal protein S17 gene (RPS17) is mutated in Diamond-Blackfan anemia. Hum. Mutat. 28:1178–1182.
   PubMed Web of Science ®Google Scholar
• Copp, A. J., F. A. Brook, and H. J. Roberts. 1988. A cell-type-specific abnormality of cell proliferation in mutant (curly tail) mouse embryos developing spinal neural tube defects. Development 104:285–295.
   PubMedGoogle Scholar
• Draptchinskaia, N., P. Gustavsson, B. Andersson, M. Pettersson, T. N. Willig, I. Dianzani, S. Ball, G. Tchernia, J. Klar, H. Matsson, D. Tentler, N. Mohandas, B. Carlsson, and N. Dahl. 1999. The gene encoding ribosomal protein S19 is mutated in Diamond-Blackfan anaemia. Nat. Genet. 21:169–175.
   PubMed Web of Science ®Google Scholar
• Dresios, J., I. L. Derkatch, S. W. Liebman, and D. Synetos. 2000. Yeast ribosomal protein L24 affects the kinetics of protein synthesis and ribosomal protein L39 improves translational accuracy, while mutants lacking both remain viable. Biochemistry 39:7236–7244.
   PubMed Web of Science ®Google Scholar
• Ebert, B. L., J. Pretz, J. Bosco, C. Y. Chang, P. Tamayo, N. Galili, A. Raza, D. E. Root, E. Attar, S. R. Ellis, and T. R. Golub. 2008. Identification of RPS14 as a 5q− syndrome gene by RNA interference screen. Nature 451:335–339.
   PubMed Web of Science ®Google Scholar
• Farrar, J. E., M. Nater, E. Caywood, M. A. McDevitt, J. Kowalski, C. M. Takemoto, C. C. Talbot, Jr., P. Meltzer, D. Esposito, A. H. Beggs, H. E. Schneider, A. Grabowska, S. E. Ball, E. Niewiadomska, C. A. Sieff, A. Vlachos, E. Atsidaftos, S. R. Ellis, J. M. Lipton, H. T. Gazda, and R. J. Arceci. 2008. Abnormalities of the large ribosomal subunit protein, Rpl35a, in Diamond-Blackfan anemia. Blood 112:1582–1592.
   PubMed Web of Science ®Google Scholar
• Fatica, A., and D. Tollervey. 2002. Making ribosomes. Curr. Opin. Cell Biol. 14:313–318.
   PubMed Web of Science ®Google Scholar
• Feng, Z., H. Zhang, A. J. Levine, and S. Jin. 2005. The coordinate regulation of the p53 and mTOR pathways in cells. Proc. Natl. Acad. Sci. USA 102:8204–8209.
   PubMed Web of Science ®Google Scholar
• Ferreira-Cerca, S., G. Poll, P. E. Gleizes, H. Tschochner, and P. Milkereit. 2005. Roles of eukaryotic ribosomal proteins in maturation and transport of pre-18S rRNA and ribosome function. Mol. Cell 20:263–275.
   PubMed Web of Science ®Google Scholar
• Garcia-Cao, I., M. Garcia-Cao, J. Martin-Caballero, L. M. Criado, P. Klatt, J. M. Flores, J. C. Weill, M. A. Blasco, and M. Serrano. 2002. “Super p53” mice exhibit enhanced DNA damage response, are tumor resistant and age normally. EMBO J. 21:6225–6235.
   PubMed Web of Science ®Google Scholar
• Gazda, H. T., A. Grabowska, L. B. Merida-Long, E. Latawiec, H. E. Schneider, J. M. Lipton, A. Vlachos, E. Atsidaftos, S. E. Ball, K. A. Orfali, E. Niewiadomska, L. Da Costa, G. Tchernia, C. Niemeyer, J. J. Meerpohl, J. Stahl, G. Schratt, B. Glader, K. Backer, C. Wong, D. G. Nathan, A. H. Beggs, and C. A. Sieff. 2006. Ribosomal protein S24 gene is mutated in Diamond-Blackfan anemia. Am. J. Hum. Genet. 79:1110–1118.
   PubMed Web of Science ®Google Scholar
• Gazda, H. T., M. R. Sheen, A. Vlachos, V. Choesmel, M. F. O'Donohue, H. Schneider, N. Darras, C. Hasman, C. A. Sieff, P. E. Newburger, S. E. Ball, E. Niewiadomska, M. Matysiak, J. M. Zaucha, B. Glader, C. Niemeyer, J. J. Meerpohl, E. Atsidaftos, J. M. Lipton, P. E. Gleizes, and A. H. Beggs. 2008. Ribosomal protein L5 and L11 mutations are associated with cleft palate and abnormal thumbs in Diamond-Blackfan anemia patients. Am. J. Hum. Genet. 83:769–780.
   PubMed Web of Science ®Google Scholar
• Gilbert, S. F. 2003. Developmental biology, 7th ed. Sinauer Associates, Inc., Sunderland, MA.
   Google Scholar
• Gottlieb, E., R. Haffner, A. King, G. Asher, P. Gruss, P. Lonai, and M. Oren. 1997. Transgenic mouse model for studying the transcriptional activity of the p53 protein: age- and tissue-dependent changes in radiation-induced activation during embryogenesis. EMBO J. 16:1381–1390.
   PubMedGoogle Scholar
• Jacks, T., L. Remington, B. O. Williams, E. M. Schmitt, S. Halachmi, R. T. Bronson, and R. A. Weinberg. 1994. Tumor spectrum analysis in p53-mutant mice. Curr. Biol. 4:1–7.
   PubMed Web of Science ®Google Scholar
• Jones, N. C., M. L. Lynn, K. Gaudenz, D. Sakai, K. Aoto, J. P. Rey, E. F. Glynn, L. Ellington, C. Du, J. Dixon, M. J. Dixon, and P. A. Trainor. 2008. Prevention of the neurocristopathy Treacher Collins syndrome through inhibition of p53 function. Nat. Med. 14:125–133.
   PubMed Web of Science ®Google Scholar
• Komarov, P. G., E. A. Komarova, R. V. Kondratov, K. Christov-Tselkov, J. S. Coon, M. V. Chernov, and A. V. Gudkov. 1999. A chemical inhibitor of p53 that protects mice from the side effects of cancer therapy. Science 285:1733–1737.
   PubMed Web of Science ®Google Scholar
• Komarova, E. A., M. V. Chernov, R. Franks, K. Wang, G. Armin, C. R. Zelnick, D. M. Chin, S. S. Bacus, G. R. Stark, and A. V. Gudkov. 1997. Transgenic mice with p53-responsive lacZ: p53 activity varies dramatically during normal development and determines radiation and drug sensitivity in vivo. EMBO J. 16:1391–1400.
   PubMed Web of Science ®Google Scholar
• Kruiswijk, T., R. J. Planta, and J. M. Krop. 1978. The course of the assembly of ribosomal subunits in yeast. Biochim. Biophys. Acta 517:378–389.
   PubMedGoogle Scholar
• Lohrum, M. A., R. L. Ludwig, M. H. Kubbutat, M. Hanlon, and K. H. Vousden. 2003. Regulation of HDM2 activity by the ribosomal protein L11. Cancer Cell 3:577–587.
   PubMed Web of Science ®Google Scholar
• Lowe, S. W., E. M. Schmitt, S. W. Smith, B. A. Osborne, and T. Jacks. 1993. p53 is required for radiation-induced apoptosis in mouse thymocytes. Nature 362:847–849.
   PubMed Web of Science ®Google Scholar
• Marion, M. J., and C. Marion. 1987. Localization of ribosomal proteins on the surface of mammalian 60S ribosomal subunits by means of immobilized enzymes: correlation with chemical cross-linking data. Biochem. Biophys. Res. Commun. 149:1077–1083.
   PubMed Web of Science ®Google Scholar
• McGowan, K. A., J. Z. Li, C. Y. Park, V. Beaudry, H. K. Tabor, A. J. Sabnis, W. Zhang, H. Fuchs, M. H. de Angelis, R. M. Myers, L. D. Attardi, and G. S. Barsh. 2008. Ribosomal mutations cause p53-mediated dark skin and pleiotropic effects. Nat. Genet. 40:963–970.
   PubMed Web of Science ®Google Scholar
• Mendez-Vidal, C., M. T. Wilhelm, F. Hellborg, W. Qian, and K. G. Wiman. 2002. The p53-induced mouse zinc finger protein wig-1 binds double-stranded RNA with high affinity. Nucleic Acids Res. 30:1991–1996.
   PubMedGoogle Scholar
• Nagy, A., M. Gertsenstein, K. Vintersten, and R. Behringer. 2003. Manipulating the mouse embryo: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
   Google Scholar
• Nikolaev, A. Y., M. Li, N. Puskas, J. Qin, and W. Gu. 2003. Parc: a cytoplasmic anchor for p53. Cell 112:29–40.
   PubMed Web of Science ®Google Scholar
• Nonn, L., R. R. Williams, R. P. Erickson, and G. Powis. 2003. The absence of mitochondrial thioredoxin 2 causes massive apoptosis, exencephaly, and early embryonic lethality in homozygous mice. Mol. Cell. Biol. 23:916–922.
   PubMed Web of Science ®Google Scholar
• Oliver, E. R., T. L. Saunders, S. A. Tarle, and T. Glaser. 2004. Ribosomal protein L24 defect in belly spot and tail (Bst), a mouse Minute. Development 131:3907–3920.
   PubMedGoogle Scholar
• Page, D. C., R. Mosher, E. M. Simpson, E. M. Fisher, G. Mardon, J. Pollack, B. McGillivray, A. de la Chapelle, and L. G. Brown. 1987. The sex-determining region of the human Y chromosome encodes a finger protein. Cell 51:1091–1104.
   PubMed Web of Science ®Google Scholar
• Panic, L., J. Montagne, M. Cokaric, and S. Volarevic. 2007. S6-haploinsufficiency activates the p53 tumor suppressor. Cell Cycle 6:20–24.
   PubMed Web of Science ®Google Scholar
• Panic, L., S. Tamarut, M. Sticker-Jantscheff, M. Barkic, D. Solter, M. Uzelac, K. Grabusic, and S. Volarevic. 2006. Ribosomal protein S6 gene haploinsufficiency is associated with activation of a p53-dependent checkpoint during gastrulation. Mol. Cell. Biol. 26:8880–8891.
   PubMed Web of Science ®Google Scholar
• Pestov, D. G., Z. Strezoska, and L. F. Lau. 2001. Evidence of p53-dependent cross-talk between ribosome biogenesis and the cell cycle: effects of nucleolar protein Bop1 on G1/S transition. Mol. Cell. Biol. 21:4246–4255.
   PubMed Web of Science ®Google Scholar
• Ray, P. S., A. Arif, and P. L. Fox. 2007. Macromolecular complexes as depots for releasable regulatory proteins. Trends Biochem. Sci. 32:158–164.
   PubMed Web of Science ®Google Scholar
• Rice, D. S., Q. Tang, R. W. Williams, B. S. Harris, M. T. Davisson, and D. Goldowitz. 1997. Decreased retinal ganglion cell number and misdirected axon growth associated with fissure defects in Bst/+ mutant mice. Investig. Ophthalmol. Vis. Sci. 38:2112–2124.
   PubMedGoogle Scholar
• Rubbi, C. P., and J. Milner. 2003. Disruption of the nucleolus mediates stabilization of p53 in response to DNA damage and other stresses. EMBO J. 22:6068–6077.
   PubMed Web of Science ®Google Scholar
• Rudra, D., and J. R. Warner. 2004. What better measure than ribosome synthesis? Genes Dev. 18:2431–2436.
   PubMed Web of Science ®Google Scholar
• Ruggero, D., and P. P. Pandolfi. 2003. Does the ribosome translate cancer? Nat. Rev. Cancer 3:179–192.
   PubMed Web of Science ®Google Scholar
• Sah, V. P., L. D. Attardi, G. J. Mulligan, B. O. Williams, R. T. Bronson, and T. Jacks. 1995. A subset of p53-deficient embryos exhibit exencephaly. Nat. Genet. 10:175–180.
   PubMed Web of Science ®Google Scholar
• Saveanu, C., A. Namane, P. E. Gleizes, A. Lebreton, J. C. Rousselle, J. Noaillac-Depeyre, N. Gas, A. Jacquier, and M. Fromont-Racine. 2003. Sequential protein association with nascent 60S ribosomal particles. Mol. Cell. Biol. 23:4449–4460.
   PubMed Web of Science ®Google Scholar
• Schmid, P., A. Lorenz, H. Hameister, and M. Montenarh. 1991. Expression of p53 during mouse embryogenesis. Development 113:857–865.
   PubMed Web of Science ®Google Scholar
• Schmidt, E. V. 1999. The role of c-myc in cellular growth control. Oncogene 18:2988–2996.
   PubMed Web of Science ®Google Scholar
• Sherr, C. J., and J. M. Roberts. 1999. CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev. 13:1501–1512.
   PubMed Web of Science ®Google Scholar
• Spritz, R. A., S. A. Holmes, R. Ramesar, J. Greenberg, D. Curtis, and P. Beighton. 1992. Mutations of the KIT (mast/stem cell growth factor receptor) proto-oncogene account for a continuous range of phenotypes in human piebaldism. Am. J. Hum. Genet. 51:1058–1065.
   PubMedGoogle Scholar
• Sulic, S., L. Panic, M. Barkic, M. Mercep, M. Uzelac, and S. Volarevic. 2005. Inactivation of S6 ribosomal protein gene in T lymphocytes activates a p53-dependent checkpoint response. Genes Dev. 19:3070–3082.
   PubMed Web of Science ®Google Scholar
• Tang, Q., D. S. Rice, and D. Goldowitz. 1999. Disrupted retinal development in the embryonic belly spot and tail mutant mouse. Dev. Biol. 207:239–255.
   PubMedGoogle Scholar
• Tian, H., E. K. Wittmack, and T. J. Jorgensen. 2000. p21WAF1/CIP1 antisense therapy radiosensitizes human colon cancer by converting growth arrest to apoptosis. Cancer Res. 60:679–684.
   PubMed Web of Science ®Google Scholar
• Vogelstein, B., D. Lane, and A. J. Levine. 2000. Surfing the p53 network. Nature 408:307–310.
   PubMed Web of Science ®Google Scholar
• Volarevic, S., M. J. Stewart, B. Ledermann, F. Zilberman, L. Terracciano, E. Montini, M. Grompe, S. C. Kozma, and G. Thomas. 2000. Proliferation, but not growth, blocked by conditional deletion of 40S ribosomal protein S6. Science 288:2045–2047.
   PubMed Web of Science ®Google Scholar
• Vousden, K. H., and X. Lu. 2002. Live or let die: the cell's response to p53. Nat. Rev. Cancer 2:594–604.
   PubMed Web of Science ®Google Scholar
• Watson, K. L., K. D. Konrad, D. F. Woods, and P. J. Bryant. 1992. Drosophila homolog of the human S6 ribosomal protein is required for tumor suppression in the hematopoietic system. Proc. Natl. Acad. Sci. USA 89:11302–11306.
   PubMedGoogle Scholar
• Wool, I. G. 1996. Extraribosomal functions of ribosomal proteins. Trends Biochem. Sci. 21:164–165.
   PubMed Web of Science ®Google Scholar
• Yuan, B., R. Latek, M. Hossbach, T. Tuschl, and F. Lewitter. 2004. siRNA Selection Server: an automated siRNA oligonucleotide prediction server. Nucleic Acids Res. 32:W130–W134.
   PubMed Web of Science ®Google Scholar
• Yuan, X., Y. Zhou, E. Casanova, M. Chai, E. Kiss, H. J. Grone, G. Schutz, and I. Grummt. 2005. Genetic inactivation of the transcription factor TIF-IA leads to nucleolar disruption, cell cycle arrest, and p53-mediated apoptosis. Mol. Cell 19:77–87.
   PubMed Web of Science ®Google Scholar
• Zhai, W., and L. Comai. 2000. Repression of RNA polymerase I transcription by the tumor suppressor p53. Mol. Cell. Biol. 20:5930–5938.
   PubMed Web of Science ®Google Scholar
• Zhang, Y., G. W. Wolf, K. Bhat, A. Jin, T. Allio, W. A. Burkhart, and Y. Xiong. 2003. Ribosomal protein L11 negatively regulates oncoprotein MDM2 and mediates a p53-dependent ribosomal-stress checkpoint pathway. Mol. Cell. Biol. 23:8902–8912.
   PubMed Web of Science ®Google Scholar
• Zhao, L., T. Samuels, S. Winckler, C. Korgaonkar, V. Tompkins, M. C. Horne, and D. E. Quelle. 2003. Cyclin G1 has growth inhibitory activity linked to the ARF-Mdm2-p53 and pRb tumor suppressor pathways. Mol. Cancer Res. 1:195–206.
   PubMed Web of Science ®Google Scholar