Loss of ribosomal protein L11 affects zebrafish embryonic development through a p53-dependent apoptotic response

PLoS ONE

Volumn 4, Issue 1, 2009, Pages

  Chakraborty, Anirban ^a   Uechi, Tamayo ^a   Higa, Sayomi ^a   Torihara, Hidetsugu ^a   Kenmochi, Naoya ^a  

^a UNIVERSITY OF MIYAZAKI   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; PROTEIN L 11; PROTEIN P53; RIBOSOME PROTEIN; UNCLASSIFIED DRUG; RIBOSOMAL PROTEIN L11; TRANSCRIPTION FACTOR; ZEBRAFISH PROTEIN;

APOPTOSIS; ARTICLE; BRAIN DEVELOPMENT; BRAIN DISEASE; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; FERTILIZATION; GENE DELETION; IN SITU HYBRIDIZATION; LETHALITY; NEURAL STEM CELL; NICK END LABELING; NONHUMAN; PROTEIN DEPLETION; PROTEIN FUNCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; WESTERN BLOTTING; ZEBRA FISH; ANIMAL; ANIMAL EMBRYO; GENETICS; METABOLISM; NERVE CELL; PRENATAL DEVELOPMENT; SIGNAL TRANSDUCTION; TRANSGENIC ANIMAL;

ANIMALIA; DANIO RERIO;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; APOPTOSIS; EMBRYO, NONMAMMALIAN; EMBRYONIC DEVELOPMENT; NEURONS; RIBOSOMAL PROTEINS; RNA, MESSENGER; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEIN P53; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 58349108899     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0004152     Document Type: Article

References (50)

1. Wool IG (1979) The structure and function of eukaryotic ribosomes. Annu Rev Biochem 48: 719-754.
2. Kenmochi N (2003) Ribosomes and ribosomal proteins. In: Cooper D, ed. Nature Encyclopedia of The Human Genome. London: Nature Publishing Group 5: 77-82.
3. Stern S, Powers T, Changchien LM, Noller HF (1989) RNA-protein interactions in 30S ribosomal subunits: folding and function of 16S rRNA. Science 244: 783-790.
4. Wool IG (1996) Extraribosomal functions of ribosomal proteins. Trends Biochem Sci 21: 164-165.
5. Soulet F, Al Saati T, Roga S, Amalric F, Bouche G (2001) Fibroblast growth factor-2 interacts with free ribosomal protein S19. Biochem Biophys Res Commun 289: 591-596.
6. Noller HF (2005) RNA structure: reading the ribosome. Science 309: 1508-1514.
7. Klein DJ, Moore PB, Steitz TA (2004) The role of ribosomal proteins in the structure assembly, and evolution of the large ribosomal subunit. J Mol Biol 340: 141-177.
8. Lambertsson A (1998) The Minute genes in Drosophila and their molecular functions. Adv Genet 38: 69-134.
9. Marygold S, Roote J, Reuter G, Lambertsson A, Ashburner M, et al. (2007) The ribosomal protein genes and Minute loci of Drosophila melanogaster. Genome Biol 8: R216.
10. Oliver ER, Saunders TL, Tarlé SA, Glaser T (2004) Ribosomal protein L24 defect in belly spot and tail (Bst), a mouse Minute. Development 131: 3907-3920.
11. Amsterdam A, Sadler KC, Lai K, Farrington S, Bronson RT, et al. (2004) Many ribosomal protein genes are cancer genes in zebrafish. PLoS Biol 2: el39.
12. Draptchinskaia N, Gustavsson P, Andersson B, Pettersson M, Willig TN, et al. (1999) The gene encoding ribosomal protein S19 is mutated in Diamond-Blackfan anemia. Nat Genet 21: 169-175.
13. Gazda HT, Grabowska A, Merida-Long LB, Latawiec E, Schneider HE, et al. (2006) Ribosomal protein S24 gene is mutated in Diamond-Blackfan anemia. Am J Hum Genet 79: 1110-1118.
14. Cmejla R, Cmejlova J, Handrkova H, Petrak J, Pospisilova D (2007) Ribosomal protein S17 gene (RPS17) is mutated in Diamond-Blackfan anemia. Hum Mutat 0: 1-5.
15. Farrar JE, Nater M, Caywood E, McDevitt MA, Kowalski J, et al. (2008) Abnormalities of the large ribosomal subunit protein Rpl35a in Diamond-Blackfan anemia. Blood 112: 1582-1592.
16. Ebert BL, Pretz J, Bosco J, Chang CY, Tamayo P, et al. (2008) Identification of RPS14 as a 5q syndrome gene by RNA interference screen. Nature 451: 335-340.
17. Uechi T, Nakajima Y, Nakao A, Torihara H, Chakraborty A, et al. (2006) Ribosomal protein gene knockdown causes developmental defects in zebrafish. PLoS ONE 1: e37.
18. Uechi T, Nakajima Y, Chakraborty A, Torihara H, Higa S, et al. (2008) Deficiency of ribosomal protein S19 during early embryogenesis leads to reduction of erthrocytes in a zebrafish model of Diamond-Blackfan anemia. Human Mol Genet 17: 3204-3211.
19. Zhang Y, Wolf GW, Bhat K, Jin A, Allio T, et al. (2003) Ribosomal protein L11 negatively regulates oncoprotein MDM2 and mediates a p53-dependent ribosomal-stress checkpoint pathway. Mol Cell Biol 23: 8902-8912.
20. 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.
21. 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.
22. Vogelstein B, Lane D, Levine A (2000) Surfing the p53 network. Nature 408: 307-310.
23. Ryan KM, Phillips AC, Vousden KH (2001) Regulation and function of the p53 tumor suppressor protein. Curr Opin Cell Biol 13: 332-337.
24. Strezoska Ž, Pestov DG, Lester FL (2002) Functional Inactivation of the Mouse Nucleolar Protein Bop1 Inhibits Multiple Steps in Pre-rRNA Processing and Blocks Cell Cycle Progression. J Biol Chem 277: 29617-29625.
25. Oeffinger M, Leung A, Lamond A, Tollervey D, Leung A (2002) Yeast Pescadillo is required for multiple activities during 60S ribosomal subunit synthesis RNA 8: 626-636.
26. Azuma M, Toyama R, Laver E, Dawid IB (2006) Perturbation of rRNA synthesis in the bap28 mutation leads to apoptosis mediated by p53 in the zebrafish central nervous system. J Biol Chem 281: 13309-13316.
27. Leary DJ, Huang S (2001) Regulation of ribosome biogenesis within the nucleolus. FEBS Lett 509: 145-150.
28. Rubbi CP, Milner J (2003) Disruption of the nucleolus mediates stabilization of p53 in response to DNA damage and other stresses. EMBO J 22: 6068-6077.
29. Heisenberg CP, Brennan C, Wilson SW (1999) Zebrafish aussicht mutant embryos exhibit widespread overexpression of ace (fgf8) and coincident defects in CNS development. Development 126: 2129-2140.
30. Cole LK, Ross LS (2001) Apoptosis in the developing zebrafish embryo. Dev Biol 240: 123-142.
31. Langheinrich U, Hennen E, Stott G, Vacun G (2002) Zebrafish as a model organism for the identification and characterization of drugs and genes affecting p53 signalling. Curr Biol 12: 2023-2028.
32. Marechal V, Elenbaas B, Piette J, Nicolas JC, Levine AJ (1994) The ribosomal protein L5 is associated with mdm-2 and mdm-2-p53 complexes. Mol Cell Biol 14: 7414-7420.
33. Dai M, Zeng SX, Jin Y, Sun X, David L, et al. (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.
34. Sun X, Dai MS, Lu H (2008) Mycophenolic acid activation of p53 requires ribosomal proteins L5 and L11. J Biol Chem 283: 12387-12392.
35. Dai M, Shi D, Jin Y, Sun X, Zhang Y, Grossman S, et al. (2006) Regulation of the MDM2-p53 pathway by ribosomal protein L11 involves a post-ubiquitination mechanism. J Biol Chem 281: 24304-24313.
36. Robu ME, Larson JD, Nasevicius A, Beiraghi S, Brenner C, et al. (2007) p53 activation by knockdown technologies. PLoS Genet 3: e78.
37. Amsterdam A, Nissen RM, Sun Z, Swindell EC, Farrington S, et al. (2004) Identification of 315 genes essential for early zebrafish development. Proc Natl Acad Sci USA 101: 12792-12797.
38. Danilova N, Sakamoto KM, Lin S (2008) Ribosomal protein S19 deficiency in zebrafish leads to developmental abnormalities and defective erythropoeisis through activation of p53 protein family. Blood in press.
39. Skarie JM, Link BA (2008) The primary open-angle glaucoma gene WDR36 functions in ribosomal-RNA processing and interacts with the p53 stress-response pathway. Hum. Mol Genet in press.
40. McGowan KA, Li JZ, Park CY, Beaudry V, Tabor HK, et al. (2008) Ribosomal mutations cause p53-mediated dark skin and pleiotrophic effects. Nature Genet in press.
41. Panić L, Tamarut S, Sticker-Jantscheff M, Barkić M, Solter D, et al. (2006) Ribosomal protein S6 gene haploinsufficiency is associated with activation of a p53-dependent checkpoint during gastrulation. Mol Cell Biol 26: 8880-8891.
42. Anderson SJ, Lauritsen JPH, Hartman MG, DiGeorge Foushee AM, Lefebvre JM, et al. (2007) Ablation of ribosomal protein L22 selectively impairs αβ T cell development by activation of a p53-dependent checkpoint. Immunity 26: 759-772.
43. Chen J, Ruan H, Ng SM, Gao C, Soo HM, et al. (2005) Loss of function of def selectively up-regulates Δ113p53 expression to arrest expansion growth of digestive organs in zebrafish. Genes and Dev 19: 2900-2911.
44. Opferman JT, Zambetti GP (2006) Translational research? Ribosome integrity and a new p53 tumor suppressor checkpoint. Cell Death and Differ 13: 898-901.
45. Boisvert FM, van Koningsbruggen S, Navascues J, Lamond AI (2007) The multifunctional nucleolus. Nat Rev Mol Cell Biol 8: 574-585.
46. Miyoshi K, Shirai C, Horigome C, Takenami K, Kawasaki J, et al. (2004) Rrs1p, a ribosomal protein L11-binding protein, is required for nuclear export of the 60S pre-ribosomal subunit in Saccharomyces cerevisiae. FEBS Lett 565: 106-110.
47. ZFIN: The Zebrafish Model Organism Database (http://zfin.org). Accessed 2008 Sep 10.
48. Maclnnes AW, Amsterdam A, Whittaker CA, Hopkins N, Lees JA (2008) Loss of p53 synthesis in zebrafish tumors with ribosomal protein gene mutations. Proc Natl Acad Sci USA 105: 10408-10413.
49. Berghmans S, Murphey RD, Wienholds E, Neuberg D, Kutok JL, et al. (2005) tp53 mutant zebrafish develop malignant peripheral nerve sheath tumors. Proc Natl Acad Sci USA 102: 407-412.
50. Thisse B, Thisse C (2004) Fast Release Clones: A high throughput expression analysis. Available at: http://zfin.org. Accessed 2008 Sep 10.