Ribosome profiling reveals a cell-type-specific translational landscape in brain tumors

Journal of Neuroscience

Volumn 34, Issue 33, 2014, Pages 10924-10936

  Gonzalez, Christian ^a   Sims, Jennifer S ^a   Hornstein, Nicholas ^a   Mela, Angeliki ^a   Garcia, Franklin ^a   Lei, Liang ^a   Gass, David A ^a   Amendolara, Benjamin ^a   Bruce, Jeffrey N ^a   Canoll, Peter ^a   Sims, Peter A ^a  

^a NewYork Presbyterian Hospital   (United States)

Author keywords

Cell type specific expression; Glioblastoma; Glioma; Ribosome profiling; Translational regulation

Indexed keywords

ALLOGRAFT INFLAMMATORY FACTOR 1; CRE RECOMBINASE; HERMES ANTIGEN; PANCREATIC RIBONUCLEASE; PLATELET DERIVED GROWTH FACTOR B;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOINFORMATICS; BRAIN TUMOR; CELL TYPE; CLINICAL ARTICLE; CONTROLLED STUDY; ENVIRONMENTAL ENRICHMENT; EPIFLUORESCENCE MICROSCOPY; EXON; FEMALE; GENE EXPRESSION PROFILING; GENE ONTOLOGY; GENE OVEREXPRESSION; GENETIC ASSOCIATION; GLIOMA; HUMAN; HUMAN TISSUE; IMMUNOFLUORESCENCE TEST; IMMUNOPRECIPITATION; MICROGLIA; MOUSE; MRNA EXPRESSION ASSAY; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RETROVIRUS; RNA EXTRACTION; RNA SEQUENCE; SEQUENCE ANALYSIS; TRANSLATION REGULATION; TUMOR MICROENVIRONMENT; UPREGULATION; ANIMAL; BRAIN; CELL TRANSFORMATION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; RIBOSOME;

ANIMALS; BRAIN; BRAIN NEOPLASMS; CELL TRANSFORMATION, NEOPLASTIC; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOMA; HUMANS; MICE; RIBOSOMES;

EID: 84905836835     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0084-14.2014     Document Type: Article

References (38)

1. Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11:R106.CrossRef Medline
2. Arribere JA, Gilbert WV (2013) Roles for transcript leaders in translation and mRNA decay revealed by transcript leader sequencing. Genome Res 23:977-987.CrossRef Medline
3. Assanah M, Lochhead R, Ogden A, Bruce J, Goldman J, Canoll P (2006) Glial progenitors in adult white matter are driven to form malignant gliomas by platelet-derived growth factor-expressing retroviruses. J Neurosci 26:6781-6790.CrossRef Medline
4. Barbosa C, Peixeiro I, Romão L (2013) Gene expression regulation by upstream open reading frames and human disease. PLoS Genet 9:e1003529.CrossRef Medline
5. Bédard A, Tremblay P, Chernomoretz A, Vallières L (2007) Identification of genes preferentially expressed by microglia and upregulated during cuprizone-induced inflammation. Glia 55:777-789.CrossRef Medline
6. Berriz GF, Beaver JE, Cenik C, Tasan M, Roth FP (2009) Next generation software for functional trend analysis. Bioinformatics 25:3043-3044.CrossRef Medline
7. Bonavia R, Inda MM, Cavenee WK, Furnari FB (2011) Heterogeneity maintenance in glioblastoma: a social network. Cancer Res 71:4055-4060.CrossRef Medline
8. Brar GA, Yassour M, Friedman N, Regev A, Ingolia NT, Weissman JS (2012) High-resolution view of the yeast meiotic program revealed by ribosome profiling. Science 335:552-557.CrossRef Medline
9. Cahoy JD, Emery B, Kaushal A, Foo LC, Zamanian JL, Christopherson KS, Xing Y, Lubischer JL, Krieg PA, Krupenko SA, Thompson WJ, Barres BA (2008) A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J Neurosci 28:264-278.CrossRef Medline
10. Chen Z, Trotman LC, Shaffer D, Lin HK, Dotan ZA, Niki M, Koutcher JA, Scher HI, Ludwig T, Gerald W, Cordon-Cardo C, Pandolfi PP (2005) Crucial role of p53-dependent cellular senescence in suppression of Ptendeficient tumorigenesis. Nature 436:725-730.CrossRef Medline
11. Doyle JP, Dougherty JD, Heiman M, Schmidt EF, Stevens TR, Ma G, Bupp S, Shrestha P, Shah RD, Doughty ML, Gong S, Greengard P, Heintz N (2008) Application of a translational profiling approach for the comparative analysis of CNS cell types. Cell 135:749-762.CrossRef Medline
12. Fan QW, Cheng CK, Nicolaides TP, Hackett CS, Knight ZA, Shokat KM, Weiss WA (2007) A dual phosphoinositide-3-kinase alpha/mTOR inhibitor cooperates with blockade of epidermal growth factor receptor in PTEN-mutant glioma. Cancer Res 67:7960-7965.CrossRef Medline
13. Goodarzi H, Elemento O, Tavazoie S (2009) Revealing global regulatory perturbations across human cancers. Mol Cell 36:900-911.CrossRef Medline
14. Heiman M, Schaefer A, Gong S, Peterson JD, Day M, Ramsey KE, Suárez-Farinas M, Schwarz C, Stephan DA, Surmeier DJ, Greengard P, Heintz N (2008) A translational profiling approach for the molecular characterization of CNS cell types. Cell 135:738-748.CrossRef Medline
15. Helmy K, Halliday J, Fomchenko E, Setty M, Pitter K, Hafemeister C, Holland EC (2012) Identification of global alteration of translational regulation in glioma in vivo. PLoS One 7:e46965.CrossRef Medline
16. Hoelzinger DB, Demuth T, Berens ME (2007) Autocrine factors that sustain glioma invasion and paracrine biology in the brain microenvironment. J Natl Cancer Inst 99:1583-1593.CrossRef Medline
17. Hsieh AC, Liu Y, Edlind MP, Ingolia NT, Janes MR, Sher A, Shi EY, Stumpf CR, Christensen C, Bonham MJ, Wang S, Ren P, Martin M, Jessen K, Feldman ME, Weissman JS, Shokat KM, Rommel C, Ruggero D (2012) The translational landscape of mTOR signalling steers cancer initiation and metastasis. Nature 485:55-61.CrossRef Medline
18. Ingolia NT, Ghaemmaghami S, Newman JR, Weissman JS (2009) Genomewide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 324:218-223.CrossRef Medline
19. Ingolia NT, Lareau LF, Weissman JS (2011) Ribosome profiling of mouse embryonic stem cells reveals the complexity and dynamics of mammalian proteomes. Cell 147:789-802.CrossRef Medline
20. Ingolia NT, Brar GA, Rouskin S, McGeachy AM, Weissman JS (2012) The ribosome profiling strategy for monitoring translation in vivo by deepsequencing of ribosome-protectedmRNAfragments. Nat Protoc 7:1534-1550.CrossRef Medline
21. Jiang BH, Liu LZ (2009) PI3K/PTEN signaling in angiogenesis and tumorigenesis. Adv Cancer Res 102:19-65.CrossRef Medline
22. Katz AM, Amankulor NM, Pitter K, Helmy K, Squatrito M, Holland EC (2012) Astrocyte-specific expression patterns associated with the PDGFinduced glioma microenvironment. PLoS One 7:e32453.CrossRef Medline
23. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14:R36.CrossRef Medline
24. Kuhn A, Thu D, Waldvogel HJ, Faull RL, Luthi-Carter R (2011) Populationspecific expression analysis (PSEA) reveals molecular changes in diseased brain. Nat Methods 8:945-947.CrossRef Medline
25. Langmead B, Salzberg SL (2012) Fast gapped-read alignment with bowtie 2. Nat Methods 9:357-359.CrossRef Medline
26. Lei L, Sonabend AM, Guarnieri P, Soderquist C, Ludwig T, Rosenfeld S, Bruce JN, Canoll P (2011) Glioblastoma models reveal the connection between adult glial progenitors and the proneural phenotype. PLoS One 6:e20041.CrossRef Medline
27. Liu C, Sage JC, Miller MR, Verhaak RG, Hippenmeyer S, Vogel H, Foreman O, Bronson RT, Nishiyama A, Luo L, Zong H (2011) Mosaic analysis with double markers reveals tumor cell of origin in glioma. Cell 146:209-221.CrossRef Medline
28. Parsa AT, Holland EC (2004) Cooperative translational control of gene expression by Ras and Akt in cancer. Trends Mol Med 10:607-613.CrossRef Medline
29. Pong WW, Gutmann DH (2011) The ecology of brain tumors: lessons learned from neurofibromatosis-1. Oncogene 30:1135-1146.CrossRef Medline
30. Rajasekhar VK, Viale A, Socci ND, Wiedmann M, Hu X, Holland EC (2003) Oncogenic Ras and Akt signaling contribute to glioblastoma formation by differential recruitment of existing mRNAs to polysomes. Mol Cell 12: 889-901.CrossRef Medline
31. Sanz E, Yang L, Su T, Morris DR, McKnight GS, Amieux PS (2009) Celltype-specific isolation of ribosome-associated mRNA from complex tissues. Proc Natl Acad Sci U S A 106:13939-13944.CrossRef Medline
32. Signer RA, Magee JA, Salic A, Morrison SJ (2014) Haematopoietic stem cells require a highly regulated protein synthesis rate. Nature 509:49-54.CrossRef Medline
33. Somers J, Pöyry T, Willis AE (2013) A perspective on mammalian upstream open reading frame function. Int J Biochem Cell Biol 45:1690-1700.CrossRef Medline
34. Sonabend AM, Yun J, Lei L, Leung R, Soderquist C, Crisman C, Gill BJ, Carminucci A, Sisti J, Castelli M, Sims PA, Bruce JN, Canoll P (2013) Murine cell line model of proneural glioma for evaluation of anti-tumor therapies. J Neurooncol 112:375-382.CrossRef Medline
35. Sonabend AM, Bansal M, Guarnieri P, Lei L, Amendolara B, Soderquist C, Leung R, Yun J, Kennedy B, Sisti J, Bruce S, Bruce R, Shakya R, Ludwig T, Rosenfeld S, Sims PA, Bruce JN, Califano A, Canoll P (2014) The transcriptional regulatory network of proneural glioma determines the genetic alterations selected during tumor progression. Cancer Res 74: 1440-1451.CrossRef Medline
36. Tahmasebi S, Alain T, Rajasekhar VK, Zhang JP, Prager-Khoutorsky M, Khoutorsky A, Dogan Y, Gkogkas CG, Petroulakis E, Sylvestre A, Ghorbani M, Assadian S, Yamanaka Y, Vinagolu-Baur JR, Teodoro JG, Kim K, Yang XJ, Sonenberg N (2014) Multifaceted regulation of somatic cell reprogramming by mRNA translational control. Cell Stem Cell 14:606-616.CrossRef Medline
37. Takeuchi H, Kondo Y, Fujiwara K, Kanzawa T, Aoki H, Mills GB, Kondo S (2005) Synergistic augmentation of rapamycin-induced autophagy in malignant glioma cells by phosphatidylinositol 3-kinase/protein kinase B inhibitors. Cancer Res 65:3336-3346.CrossRef Medline
38. Verhaak RGW, Hoadley KA, Purdom E, Wang V, Qi Y, Wilkerson MD, Miller CR, Ding L, Golub T, Mesirov JP, Alexe G, Lawrence M, O'Kelly M, Tamayo P, Weir BA, Gabriel S, Winckler W, Gupta S, Jakkula L, Feiler HS, et al. (2010) Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 17:98-110.CrossRef Medline