Tumour-specific proline vulnerability uncovered by differential ribosome codon reading

Nature

Volumn 530, Issue 7591, 2016, Pages 490-494

  Loayza Puch, Fabricio ^a   Rooijers, Koos ^a   Buil, Levi C M ^a   Zijlstra, Jelle ^a   Oude Vrielink, Joachim F ^a   Lopes, Rui ^a   Ugalde, Alejandro Pineiro ^a   Van Breugel, Pieter ^a   Hofland, Ingrid ^a   Wesseling, Jelle ^a   Van Tellingen, Olaf ^a   Bex, Axel ^a   Agami, Reuven ^a,b  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

^b ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARAGINASE; ASPARAGINE; ASPARTATE AMMONIA LIGASE; CRISPR ASSOCIATED PROTEIN; ENZYME; GLUTAMINE; GLYCINE; LEUCINE; PROLINE; PYCR1 PROTEIN; SERINE; UNCLASSIFIED DRUG; CODON; DELTA-1-PYRROLINE-5-CARBOXYLATE REDUCTASE; PYRROLINE 5 CARBOXYLATE REDUCTASE;

AMINO ACID; CANCER; CELLS AND CELL COMPONENTS; ENZYME ACTIVITY; METABOLISM; PROTEIN; TUMOR; VULNERABILITY;

AMINO ACID DEFICIENCY; AMINO ACID METABOLISM; ARTICLE; BREAST CARCINOMA; CELL PROLIFERATION; CELL SURVIVAL; CODON; CONTROLLED STUDY; ENZYME INDUCTION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; KIDNEY CANCER; METABOLIC REGULATION; PRIORITY JOURNAL; RIBOSOME; SIGNAL TRANSDUCTION; TUMOR GROWTH; ANIMAL; BIOSYNTHESIS; BREAST TUMOR; DEFICIENCY; FEMALE; GENE INACTIVATION; GENETICS; KIDNEY TUMOR; METABOLISM; MOUSE; PAGET NIPPLE DISEASE; PATHOLOGY; PROTEIN SYNTHESIS; TUMOR CELL LINE;

ANIMALS; ASPARAGINASE; ASPARAGINE; ASPARTATE-AMMONIA LIGASE; BREAST NEOPLASMS; CARCINOMA, DUCTAL, BREAST; CELL LINE, TUMOR; CELL PROLIFERATION; CODON; FEMALE; GENE KNOCKOUT TECHNIQUES; HUMANS; KIDNEY NEOPLASMS; MICE; PROLINE; PROTEIN BIOSYNTHESIS; PYRROLINE CARBOXYLATE REDUCTASES; RIBOSOMES;

EID: 84959386368     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature16982     Document Type: Article

References (30)

1. Jain, M. et al. Metabolite profiling identifies a key role for glycine in rapid cancer cell proliferation. Science 336, 1040-1044 (2012).
2. Maddocks, O. D. et al. Serine starvation induces stress and p53-dependent metabolic remodelling in cancer cells. Nature 493, 542-546 (2013).
3. Sheen, J. H., Zoncu, R., Kim, D. & Sabatini, D. M. Defective regulation of autophagy upon leucine deprivation reveals a targetable liability of human melanoma cells in vitro and in vivo. Cancer Cell 19, 613-628 (2011).
4. Son, J. et al. Glutamine supports pancreatic cancer growth through a KRAS-regulated metabolic pathway. Nature 496, 101-105 (2013).
5. Richards, N. G. & Kilberg, M. S. Asparagine synthetase chemotherapy. Annu. Rev. Biochem. 75, 629-654 (2006).
6. Ingolia, N. T., Ghaemmaghami, S., Newman, J. R. & Weissman, J. S. Genomewide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 324, 218-223 (2009).
7. De Ingeniis, J. et al. Functional specialization in proline biosynthesis of melanoma. PLoS One 7, e45190 (2012).
8. Rooijers, K., Loayza-Puch, F., Nijtmans, L. G. & Agami, R. Ribosome profiling reveals features of normal and disease-associated mitochondrial translation. Nat. Commun. 4, 2886 (2013).
9. Bazzini, A. A. et al. Identification of small ORFs in vertebrates using ribosome footprinting and evolutionary conservation. EMBO J. 33, 981-993 (2014).
10. Guydosh, N. R. & Green, R. Dom34 rescues ribosomes in 3' untranslated regions. Cell 156, 950-962 (2014).
11. Fresno, M., Carrasco, L. & Vazquez, D. Initiation of the polypeptide chain by reticulocyte cell-free systems. Survey of different inhibitors of translation. Eur. J. Biochem. 68, 355-364 (1976).
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. Zaborske, J. M. et al. Genome-wide analysis of tRNA charging and activation of the eIF2 kinase Gcn2p. J. Biol. Chem. 284, 25254-25267 (2009).
14. Singh, B. et al. Selection of metastatic breast cancer cells based on adaptability of their metabolic state. PLoS One 7, e36510 (2012).
15. Leprivier, G. et al. The eEF2 kinase confers resistance to nutrient deprivation by blocking translation elongation. Cell 153, 1064-1079 (2013).
16. Dalgliesh, G. L. et al. Systematic sequencing of renal carcinoma reveals inactivation of histone modifying genes. Nature 463, 360-363 (2010).
17. Heiman, M. et al. A translational profiling approach for the molecular characterization of CNS cell types. Cell 135, 738-748 (2008).
18. Artieri, C. G. & Fraser, H. B. Accounting for biases in riboprofiling data indicates a major role for proline in stalling translation. Genome Res. 24, 2011-2021 (2014).
19. Sabi, R. & Tuller, T. A comparative genomics study on the effect of individual amino acids on ribosome stalling. BMC Genomics 16 (Suppl. 10), S5 (2015).
20. Doerfel, L. K. et al. EF-P is essential for rapid synthesis of proteins containing consecutive proline residues. Science 339, 85-88 (2013).
21. Gutierrez, E. et al. eIF5A promotes translation of polyproline motifs. Mol. Cell 51, 35-45 (2013).
22. Loayza-Puch, F. et al. p53 induces transcriptional and translational programs to suppress cell proliferation and growth. Genome Biol. 14, R32 (2013).
23. Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal 17, 10-12 (2011).
24. Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nature Methods 9, 357-359 (2012).
25. Chan, P. P. & Lowe, T. M. GtRNAdb: a database of transfer RNA genes detected in genomic sequence. Nucleic Acids Res. 37, D93-D97 (2009).
26. Kim, D. et al. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14, R36 (2013).
27. Harrow, J. et al. GENCODE: the reference human genome annotation for The ENCODE Project. Genome Res. 22, 1760-1774 (2012).
28. Subramanian, A. et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl Acad. Sci. USA 102, 15545-15550 (2005).
29. Robinson, M. D., McCarthy, D. J. & Smyth, G. K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139-140 (2010).
30. Katz, Y., Wang, E. T., Airoldi, E. M. & Burge, C. B. Analysis and design of RNA sequencing experiments for identifying isoform regulation. Nature Methods 7, 1009-1015 (2010).