Human ribosomes from cells with reduced dyskerin levels are intrinsically altered in translation

FASEB Journal

Volumn 29, Issue 8, 2015, Pages 3472-3482

  Penzo, Marianna ^a   Rocchi, Laura ^a   Brugiere, Sabine ^b,c,d   Carnicelli, Domenica ^a   Onofrillo, Carmine ^a   Coute, Yohann ^b,c,d   Brigotti, Maurizio ^a   Montanaro, Lorenzo ^a  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b UNIV GRENOBLE ALPES   (France)

^c CEA GRENOBLE   (France)

^d INSERM   (France)

Author keywords

mRNA translation; Pseudouridylation; Ribosomal proteins

Indexed keywords

DYSKERIN; MESSENGER RNA; RIBOSOME PROTEIN; RIBOSOME RNA; URIDINE; CELL CYCLE PROTEIN; DKC1 PROTEIN, HUMAN; NUCLEAR PROTEIN;

ANIMAL CELL; ARTICLE; CELL FREE SYSTEM; CONTROLLED STUDY; DYSKERATOSIS CONGENITA; HUMAN; HUMAN CELL; INTERNAL RIBOSOME ENTRY SITE; MASS SPECTROMETRY; MOLECULAR BIOLOGY; NONHUMAN; PATHOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN SYNTHESIS; PSEUDOURIDYLATION; QUANTITATIVE ANALYSIS; RETICULOCYTE; RIBOSOME; RNA TRANSLATION; GENETICS; MCF 7 CELL LINE; METABOLISM; TELOMERE; TUMOR CELL LINE;

CELL CYCLE PROTEINS; CELL LINE, TUMOR; CELL-FREE SYSTEM; HUMANS; MCF-7 CELLS; NUCLEAR PROTEINS; PROTEIN BIOSYNTHESIS; RIBOSOMES; RNA, MESSENGER; RNA, RIBOSOMAL; TELOMERE;

EID: 84940118774     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.15-270991     Document Type: Article

References (31)

1. Kirwan, M., and Dokal, I. (2008) Dyskeratosis congenita: a genetic disorder of many faces. Clin. Genet. 73, 103-112
2. Mitchell, J. R., Wood, E., and Collins, K. (1999) A telomerase component isdefectivein the human disease dyskeratosis congenita. Nature 402, 551-555
3. Yoon, A., Peng, G., Brandenburger, Y., Zollo, O., Xu, W., Rego, E., Ruggero, D., and Ruggero, D. (2006) Impaired control of IRES-mediated translation in X-linked dyskeratosis congenita. Science 312, 902-906
4. Hellen, C. U., and Sarnow, P. (2001) Internal ribosome entry sites in eukaryotic mRNA molecules. Genes Dev. 15, 1593-1612
5. Montanaro, L., Calienni, M., Bertoni, S., Rocchi, L., Sansone, P., Storci, G., Santini, D., Ceccarelli, C., Taffurelli, M., Carnicelli, D., Brigotti, M., Bonafè, M., Treré, D., and Derenzini, M. (2010) Novel dyskerin-mediated mechanismofp53 inactivation through defective mRNA translation. Cancer Res. 70, 4767-4777
6. Rocchi, L., Pacilli, A., Sethi, R., Penzo, M., Schneider, R. J., Treré, D., Brigotti, M., and Montanaro, L. (2013) Dyskerin depletion increases VEGF mRNA internal ribosome entry site-mediated translation. Nucleic Acids Res. 41, 8308-8318
7. Jack, K., Bellodi, C., Landry, D. M., Niederer, R. O., Meskauskas, A., Musalgaonkar, S., Kopmar, N., Krasnykh, O., Dean, A. M., Thompson, S. R., Ruggero, D., and Dinman, J. D. (2011) rRNA pseudouridylation defects affect ribosomal ligand binding and translational fidelity from yeast to human cells. Mol. Cell 44, 660-666
8. Ruggero, D., Grisendi, S., Piazza, F., Rego, E., Mari, F., Rao, P. H., Cordon-Cardo, C., and Pandolfi, P. P. (2003) Dyskeratosis congenita and cancer in mice deficient in ribosomal RNA modification. Science 299, 259-262
9. Montanaro, L., Brigotti, M., Clohessy, J., Barbieri, S., Ceccarelli, C., Santini, D., Taffurelli, M., Calienni, M., Teruya-Feldstein, J., Trerè, D., Pandolfi, P. P., and Derenzini, M. (2006) Dyskerin expression influences the level of ribosomal RNA pseudo-uridylation and telomerase RNA component in human breast cancer. J. Pathol. 210, 10-18
10. Bellodi, C., Krasnykh, O., Haynes, N., Theodoropoulou, M., Peng, G., Montanaro, L., and Ruggero, D. (2010) Loss offunction of the tumor suppressor DKC1 perturbs p27 translation control and contributes to pituitary tumorigenesis. Cancer Res. 70, 6026-6035
11. Decatur, W. A., and Fournier, M. J. (2002) rRNA modifications and ribosome function. Trends Biochem. Sci. 27, 344-351
12. Dussault, A.-A., and Pouliot, M. (2006) Rapid and simple comparison of messenger RNA levels using real-time PCR. Biol. Proced. Online 8, 1-10
13. Chaudhuri, S., Vyas, K., Kapasi, P., Komar, A. A., Dinman, J. D., Barik, S., and Mazumder, B. (2007) Human ribosomal protein L13a is dispensable for canonical ribosome function but indispensable for efficient rRNA methylation. RNA 13, 2224-2237
14. Plant, E. P., Nguyen, P., Russ, J. R., Pittman, Y. R., Nguyen, T., Quesinberry, J. T., Kinzy, T. G., and Dinman, J. D. (2007) Differentiating between near- and non-cognate codons in Saccharomyces cerevisiae. PLoS ONE 2, e517
15. Marcel, V., Ghayad, S. E., Belin, S., Therizols, G., Morel, A.-P., Solano-Gonzàlez, E., Vendrell, J. A., Hacot, S., Mertani, H. C., Albaret, M. A., Bourdon, J. C., Jordan, L., Thompson, A., Tafer, Y., Cong, R., Bouvet, P., Saurin, J. C., Catez, F., Prats, A. C., Puisieux, A., and Diaz, J. J. (2013) p53 acts as a safeguard of translational control by regulating fibrillarin and rRNA methylation in cancer. Cancer Cell 24, 318-330
16. Brigotti, M., Petronini, P. G., Carnicelli, D., Alfieri, R. R., Bonelli, M. A., Borghetti, A. F., and Wheeler, K. P. (2003) Effects of osmolarity, ions and compatible osmolytes on cell-free protein synthesis. Biochem. J. 369, 369-374
17. Allen, E. H., and Schweet, R. S. (1962) Synthesis of hemoglobin in a cell-free system. I. Properties of the complete system. J. Biol. Chem. 237, 760-767
18. Morrisey, J., and Hardesty, B. (1972) Met-tRNA hydrolase from reticulocytes specific for Met-tRNA f Met on 40S ribosomal subunits. Arch. Biochem. Biophys. 152, 385-397
19. Sierra, J. M., Meier, D., and Ochoa, S. (1974) Effect of development on the translation of messenger RNA in Artemia salinaembryos. Proc. Natl. Acad. Sci. USA 71, 2693-2697
20. Cox, J., and Mann, M. (2008) MaxQuant enables high peptide identification rates, individualized p. p. b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367-1372
21. Luber, C. A., Cox, J., Lauterbach, H., Fancke, B., Selbach, M., Tschopp, J., Akira, S., Wiegand, M., Hochrein, H., O'Keeffe, M., and Mann, M. (2010) Quantitative proteomics reveals subset-specific viral recognition in dendritic cells. Immunity 32, 279-289
22. Deeb, S. J., D'Souza, R. C. J., Cox, J., Schmidt-Supprian, M., and Mann, M. (2012) Super-SILAC allows classificationofdiffuse large B-cell lymphoma subtypes by their protein expression profiles. Mol. Cell. Proteomics 11, 77-89
23. Bellodi, C., Kopmar, N., and Ruggero, D. (2010) Deregulation of oncogene-induced senescence and p53 translational control in X-linked dyskeratosis congenita. EMBO J. 29, 1865-1876
24. Thumati, N. R., Zeng, X.-L., Au, H. H. T., Jang, C. J., Jan, E., and Wong, J. M. Y. (2013) Severity of X-linked dyskeratosis congenita (DKCX) cellular defects is not directly related to dyskerin (DKC1) activity in ribosomal RNA biogenesis or mRNA translation. Hum. Mutat. 34, 1698-1707
25. Parry, E. M., Alder, J. K., Lee, S. S., Phillips III, J. A., Loyd, J. E., Duggal, P., and Armanios, M. (2011) Decreased dyskerin levels as a mechanism of telomere shortening in X-linked dyskeratosis congenita. J. Med. Genet. 48, 327-333
26. Knight, S. W., Vulliamy, T. J., Morgan, B., Devriendt, K., Mason, P. J., and Dokal, I. (2001) Identification of novel DKC1 mutations in patients with dyskeratosis congenita: implications for pathophysiology and diagnosis. Hum. Genet. 108, 299-303
27. Bellodi, C., McMahon, M., Contreras, A., Juliano, D., Kopmar, N., Nakamura, T., Maltby, D., Burlingame, A., Savage, S. A., Shimamura, A., and Ruggero, D. (2013) H/ACA small RNA dysfunctions in disease reveal key roles for noncoding RNA modifications in hematopoietic stem cell differentiation. Cell Reports 3, 1493-1502
28. Narla, A., and Ebert, B. L. (2010) Ribosomopathies: human disorders of ribosome dysfunction. Blood 115, 3196-3205
29. Narla, A., Hurst, S. N., and Ebert, B. L. (2011) Ribosome defects in disorders of erythropoiesis. Int. J. Hematol. 93, 144-149
30. Armistead, J., and Triggs-Raine, B. (2014) Diverse diseases from a ubiquitous process: the ribosomopathy paradox. FEBS Lett. 588, 1491-1500
31. Vizcáino, J. A., Deutsch, E. W., Wang, R., Csordas, A., Reisinger, F., Rios, D., Dianes, J. A., Sun, Z., Farrah, T., Bandeira, N., Binz, P.-A., Xenarios, I., Eisenacher, M., Mayer, G., Gatto, L., Campos, A., Chalkley, R. J., Kraus, H.-J., Albar, J. P., Martinez-Bartolomé, S., Apweiler, R., Omenn, G. S., Martens, L., Jones, A. R., and Hermjakob, H. (2014) ProteomeXchange provides globally coordinated proteomics data submission and dissemination. Nat. Biotechnol. 32, 223-226