DENR-MCT-1 promotes translation re-initiation downstream of uORFs to control tissue growth

Nature

Volumn 512, Issue 7513, 2014, Pages 208-212

  Schleich, Sibylle ^a,b   Strassburger, Katrin ^a   Janiesch, Philipp Christoph ^b   Koledachkina, Tatyana ^b   Miller, Katharine K ^b   Haneke, Katharina ^a,c   Cheng, Yong Sheng ^a   Küchler, Katrin ^b   Stoecklin, Georg ^a,c   Duncan, Kent E ^b   Teleman, Aurelio A ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^c UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CIS ACTING ELEMENT; DENSITY REGULATED PROTEIN; ECDYSONE RECEPTOR; INITIATION FACTOR; INSULIN RECEPTOR; MBC PROTEIN; MESSENGER RNA; MULTIPLE COPIES IN T CELL LYMPHOMA 1 PROTEIN; REGULATOR PROTEIN; TRANS ACTING FACTOR; UNCLASSIFIED DRUG;

ENZYME ACTIVITY; EUKARYOTE; MITOCHONDRIAL DNA; PROTEIN; RNA;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DROSOPHILA; GENE DOSAGE; GENE MUTATION; GENE ONTOLOGY; HUMAN; IMMUNOPRECIPITATION; MYOBLAST; NONHUMAN; OPEN READING FRAME; PHENOTYPE; POINT MUTATION; POLYSOME; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; RNA TRANSLATION; SIGNAL TRANSDUCTION; START CODON; STOP CODON; TISSUE GROWTH; TRANSLATION INITIATION; TRANSLATION REGULATION; TRANSLATION REINITIATION;

ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EUKARYOTIC INITIATION FACTORS; GENE EXPRESSION REGULATION; OPEN READING FRAMES; PROTEIN BIOSYNTHESIS; SIGNAL TRANSDUCTION;

EID: 84904974217     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature13401     Document Type: Article

References (41)

1. Jackson, R. J.,Hellen, C. U. & Pestova, T. V.Themechanismof eukaryotic translation initiation and principles of its regulation. Nature Rev. Mol. Cell Biol. 11, 113-127 (2010).
2. Sonenberg, N. & Hinnebusch, A. G. Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 136, 731-745 (2009).
3. Calvo, S. E., Pagliarini, D. J. & Mootha, V. K. Upstream open reading frames cause widespread reduction of protein expression and are polymorphicamong humans. Proc. Natl Acad. Sci. USA 106, 7507-7512 (2009).
4. Dever, T. E. & Green, R. The elongation, termination, and recycling phases of translation in eukaryotes. Cold Spring Harb. Perspect. Biol. 4, a013706 (2012).
5. Valasek, L. S. 'Ribozoomin'-translation initiation from the perspective of the ribosome-bound eukaryotic initiation factors (eIFs). Curr. Protein Pept. Sci. 13, 305-330 (2012).
6. Skabkin, M. A., Skabkina, O. V., Hellen, C. U. & Pestova, T. V. Reinitiation and other unconventional posttermination events during eukaryotic translation.Mol. Cell 51, 249-264 (2013).
7. Poyry, T. A., Kaminski, A. & Jackson, R. J. What determines whether mammalian ribosomes resume scanning after translation of a short upstream open reading frame? Genes Dev. 18, 62-75 (2004).
8. Schwanhäusser, B. et al. Global quantification of mammalian gene expression control. Nature 473, 337-342 (2011).
9. Gebauer, F. & Hentze, M. W.Molecularmechanismsof translational control. Nature Rev. Mol. Cell Biol. 5, 827-835 (2004).
10. Kong, J. & Lasko, P. Translational control in cellular and developmental processes. Nature Rev. Genet. 13, 383-394 (2012).
11. Araujo, P. R. et al. Before it gets started: regulating translation at the 59 UTR. Comp. Funct. Genomics 2012, 475731 (2012).
12. Ingolia, N. T., Lareau, L. F. & Weissman, J. S. Ribosome profiling of mouse embryonic stem cells reveals the complexity and dynamics of mammalian proteomes. Cell 147, 789-802 (2011).
13. Hinnebusch,A. G. & Lorsch, J. R.Themechanismof eukaryotic translationinitiation: new insights and challenges. Cold Spring Harb. Perspect. Biol. 4, 1-25 (2012).
14. Jackson, R. J., Hellen, C. U. & Pestova, T. V. Termination and post-termination events in eukaryotic translation. Adv. Protein Chem. Struct. Biol. 86, 45-93 (2012).
15. Somers, J., Poyry, T. & Willis, A. E. A perspective on mammalian upstream open reading frame function. Int. J. Biochem. Cell Biol. 45, 1690-1700 (2013).
16. Dmitriev, S. E. et al. GTP-independent tRNA delivery to the ribosomal P-site by a novel eukaryotic translation factor. J. Biol. Chem. 285, 26779-26787 (2010).
17. Skabkin, M. A. et al. Activities of Ligatin andMCT-1/DENR in eukaryotic translation initiation and ribosomal recycling. Genes Dev. 24, 1787-1801 (2010).
18. Dierov, J., Prosniak, M., Gallia, G. & Gartenhaus, R. B. Increased G1 cyclin/cdk activity in cells overexpressing the candidate oncogene, MCT-1. J. Cell. Biochem. 74, 544-550 (1999).
19. Mazan-Mamczarz, K. et al. Targeted suppression of MCT-1 attenuates the malignant phenotype through a translationalmechanism. Leuk. Res. 33, 474-482 (2009).
20. Prosniak, M. et al. A novel candidate oncogene, MCT-1, is involved in cell cycle progression. Cancer Res. 58, 4233-4237 (1998).
21. Kongsuwan, K. et al. A Drosophila Minute gene encodes a ribosomal protein. Nature 317, 555-558 (1985).
22. Hayashi, S., Hirose, S., Metcalfe, T. & Shirras, A. D. Control of imaginal cell development by the escargot gene of Drosophila. Development 118, 105-115 (1993).
23. Wilson, T. G., Yerushalmi, Y., Donnell, D. M. & Restifo, L. L. Interaction between hormonal signaling pathways in Drosophila melanogaster as revealed by genetic interaction between methoprene-tolerant and broad-complex. Genetics 172, 253-264 (2006).
24. Huang da, W., Sherman, B. T. & Lempicki, R. A. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 37, 1-13 (2009).
25. Bodenmiller, B. et al. PhosphoPep-a phosphoproteome resource for systems biology research in Drosophila Kc167 cells. Mol. Syst. Biol. 3, 139 (2007).
26. Nandi, S. et al. Phosphorylation of MCT-1 by p44/42 MAPK is required for its stabilization in response to DNA damage. Oncogene 26, 2283-2289 (2007).
27. Spriggs, K. A., Bushell, M. & Willis, A. E. Translational regulation of gene expression during conditions of cell stress. Mol. Cell 40, 228-237 (2010).
28. Harding, H. P. et al. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol. Cell 6, 1099-1108 (2000).
29. Vattem, K. M. & Wek, R. C. Reinitiation involving upstream ORFs regulates ATF4 mRNA translation in mammalian cells. Proc. Natl Acad. Sci. USA 101, 11269-11274 (2004).
30. Hood, H. M.,Neafsey, D. E.,Galagan, J. & Sachs, M. S. Evolutionary roles ofupstream open reading frames in mediating gene regulation in fungi. Annu. Rev. Microbiol. 63, 385-409 (2009).
31. Huang, J., Zhou, W., Watson, A. M., Jan, Y. N. & Hong, Y. Efficient ends-out gene targeting in Drosophila. Genetics 180, 703-707 (2008).
32. Erickson, M. R., Galletta, B. J. & Abmayr, S. M. Drosophila myoblast city encodes a conserved protein that is essential for myoblast fusion, dorsal closure, and cytoskeletal organization. J. Cell Biol. 138, 589-603 (1997).
33. Puig, O., Marr, M. T., Ruhf, M. L. & Tjian, R. Control of cell number by Drosophila FOXO: downstream and feedback regulation of the insulin receptor pathway. Genes Dev. 17, 2006-2020 (2003).
34. Puig, O. & Tjian, R. Transcriptional feedback control of insulin receptor by dFOXO/ FOXO1. Genes Dev. 19, 2435-2446 (2005).
35. Duncan, K. et al. Sex-lethalimparts a sex-specific function toUNRby recruiting it to themsl-2mRNA39 UTR: translational repression for dosage compensation. Genes Dev. 20, 368-379 (2006).
36. Zuker, M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31, 3406-3415 (2003).
37. Duncan, K. E., Strein, C. & Hentze, M. W. The SXL-UNR corepressor complex uses a PABP-mediated mechanismto inhibit ribosome recruitment tomsl-2mRNA. Mol. Cell 36, 571-582 (2009).
38. Gebauer, F., Corona, D. F., Preiss, T., Becker, P. B. & Hentze, M. W. Translational control of dosage compensation in Drosophila by Sex-lethal: cooperative silencing via the 59 and 39 UTRs of msl-2 mRNA is independent of the poly(A) tail. EMBO J. 18, 6146-6154 (1999).
39. Marygold, S. J. et al. FlyBase: improvements to the bibliography. Nucleic Acids Res. 41, D751-D757 (2013).
40. Cavener, D. R. Comparison of the consensus sequence flanking translational start sites in Drosophila and vertebrates. Nucleic Acids Res. 15, 1353-1361 (1987).
41. Teleman, A. A., Hietakangas, V., Sayadian, A. C. & Cohen, S. M. Nutritional control of protein biosynthetic capacity by insulin via Myc in Drosophila. Cellmetab. 7, 21-32 (2008).