Identification of Global Alteration of Translational Regulation in Glioma In Vivo

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Helmy, Karim ^a,b,c   Halliday, John ^a,d   Fomchenko, Elena ^a,e   Setty, Manu ^a   Pitter, Ken ^a,e   Hafemeister, Christoph ^f   Holland, Eric C ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^c The State University of New Jersey   (United States)

^d Gerstner Sloan Kettering Graduate School of Biomedical Sciences   (United States)

^e WEILL CORNELL MEDICAL COLLEGE   (United States)

^f NEW YORK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; OLIGODENDROCYTE TRANSCRIPTION FACTOR 2; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL CULTURE; CELL DIVISION; CELL METABOLISM; CELL POPULATION; CELL RESPIRATION; CONTROLLED STUDY; DISEASE MODEL; GENE CONTROL; GENE DELETION; GENE MUTATION; GENETIC ENGINEERING; GLIOMA; GLYCOSYLATION; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; OLIGODENDROGLIA; PROTEIN DEPLETION; REPRODUCIBILITY; RIBOSOME; RNA TRANSLATION; SIGNAL TRANSDUCTION; STEADY STATE; STEM CELL; TRANSLATION REGULATION; TUMOR CELL; TUMOR GROWTH; TUMOR SUPPRESSOR GENE;

ANIMALS; CELL RESPIRATION; CELL TRANSFORMATION, NEOPLASTIC; FEMALE; GENE DELETION; GENE EXPRESSION PROFILING; GLIOMA; MALE; MICE; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN BIOSYNTHESIS; PTEN PHOSPHOHYDROLASE; RNA, MESSENGER; RNA, RIBOSOMAL; SIGNAL TRANSDUCTION;

EID: 84867095368     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0046965     Document Type: Article

References (48)

1. Sonenberg N, Hinnebusch AG, (2009) Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 136: 731-745.
2. Le Quesne JP, Spriggs KA, Bushell M, Willis AE, (2010) Dysregulation of protein synthesis and disease. J Pathol 220: 140-151.
3. Rajasekhar VK, Holland EC, (2004) Postgenomic global analysis of translational control induced by oncogenic signaling. Oncogene 23: 3248-3264.
4. Holland EC, Sonenberg N, Pandolfi PP, Thomas G, (2004) Signaling control of mRNA translation in cancer pathogenesis. Oncogene 23: 3138-3144.
5. Rajasekhar VK, Viale A, Socci ND, Wiedmann M, Hu X, et al. (2003) Oncogenic Ras and Akt signaling contribute to glioblastoma formation by differential recruitment of existing mRNAs to polysomes. Mol Cell 12: 889-901.
6. Jackson RJ, Hellen CU, Pestova TV, (2010) The mechanism of eukaryotic translation initiation and principles of its regulation. Nat Rev Mol Cell Biol 11: 113-127.
7. Balagopal V, Parker R, (2009) Polysomes, P bodies and stress granules: states and fates of eukaryotic mRNAs. Curr Opin Cell Biol 21: 403-408.
8. Melamed D, Eliyahu E, Arava Y, (2009) Exploring translation regulation by global analysis of ribosomal association. Methods 48: 301-305.
9. Heiman M, Schaefer A, Gong S, Peterson JD, Day M, et al. (2008) A translational profiling approach for the molecular characterization of CNS cell types. Cell 135: 738-748.
10. Jones RG, Thompson CB, (2009) Tumor suppressors and cell metabolism: a recipe for cancer growth. Genes Dev 23: 537-548.
11. Kaelin WG Jr, Thompson CB, (2010) Q&A: Cancer: clues from cell metabolism. Nature 465: 562-564.
12. Plas DR, Thompson CB, (2005) Akt-dependent transformation: there is more to growth than just surviving. Oncogene 24: 7435-7442.
13. Shih AH, Dai C, Hu X, Rosenblum MK, Koutcher JA, et al. (2004) Dose-dependent effects of platelet-derived growth factor-B on glial tumorigenesis. Cancer Res 64: 4783-4789.
14. Dai C, Celestino JC, Okada Y, Louis DN, Fuller GN, et al. (2001) PDGF autocrine stimulation dedifferentiates cultured astrocytes and induces oligodendrogliomas and oligoastrocytomas from neural progenitors and astrocytes in vivo. Genes Dev 15: 1913-1925.
15. Dai C, Lyustikman Y, Shih A, Hu X, Fuller GN, et al. (2005) The characteristics of astrocytomas and oligodendrogliomas are caused by two distinct and interchangeable signaling formats. Neoplasia 7: 397-406.
16. Phillips HS, Kharbanda S, Chen R, Forrest WF, Soriano RH, et al. (2006) Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis. Cancer Cell 9: 157-173.
17. Verhaak RG, Hoadley KA, Purdom E, Wang V, Qi Y, 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.
18. Brennan C, Momota H, Hambardzumyan D, Ozawa T, Tandon A, et al. (2009) Glioblastoma subclasses can be defined by activity among signal transduction pathways and associated genomic alterations. PLoS One 4: e7752.
19. Lei L, Sonabend AM, Guarnieri P, Soderquist C, Ludwig T, et al. (2011) Glioblastoma models reveal the connection between adult glial progenitors and the proneural phenotype. PLoS One 6: e20041.
20. Charles N, Holland EC, (2010) The perivascular niche microenvironment in brain tumor progression. Cell Cycle 9: 3012-3021.
21. Doyle JP, Dougherty JD, Heiman M, Schmidt EF, Stevens TR, et al. (2008) Application of a translational profiling approach for the comparative analysis of CNS cell types. Cell 135: 749-762.
22. Fomchenko EI, Dougherty JD, Helmy KY, Katz AM, Pietras A, et al. (2011) Recruited cells can become transformed and overtake PDGF-induced murine gliomas in vivo during tumor progression. PLoS One 6: e20605.
23. Ng K, Pullirsch D, Leeb M, Wutz A, (2007) Xist and the order of silencing. EMBO Rep 8: 34-39.
24. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, et al. (2005) Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A 102: 15545-15550.
25. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, et al. (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25: 25-29.
26. Ingolia NT, Ghaemmaghami S, Newman JR, Weissman JS, (2009) Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 324: 218-223.
27. Appolloni I, Calzolari F, Tutucci E, Caviglia S, Terrile M, et al. (2009) PDGF-B induces a homogeneous class of oligodendrogliomas from embryonic neural progenitors. Int J Cancer 124: 2251-2259.
28. Rivers LE, Young KM, Rizzi M, Jamen F, Psachoulia K, et al. (2008) PDGFRA/NG2 glia generate myelinating oligodendrocytes and piriform projection neurons in adult mice. Nat Neurosci 11: 1392-1401.
29. Guo F, Ma J, McCauley E, Bannerman P, Pleasure D, (2009) Early postnatal proteolipid promoter-expressing progenitors produce multilineage cells in vivo. J Neurosci 29: 7256-7270.
30. Hanahan D, Weinberg RA, (2000) The hallmarks of cancer. Cell 100: 57-70.
31. Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, et al. (2007) The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 114: 97-109.
32. Vivanco I, Sawyers CL, (2002) The phosphatidylinositol 3-Kinase AKT pathway in human cancer. Nat Rev Cancer 2: 489-501.
33. Ma XM, Blenis J, (2009) Molecular mechanisms of mTOR-mediated translational control. Nat Rev Mol Cell Biol 10: 307-318.
34. Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 455: 1061-1068.
35. Bleau AM, Hambardzumyan D, Ozawa T, Fomchenko EI, Huse JT, et al. (2009) PTEN/PI3K/Akt pathway regulates the side population phenotype and ABCG2 activity in glioma tumor stem-like cells. Cell Stem Cell 4: 226-235.
36. Huse JT, Brennan C, Hambardzumyan D, Wee B, Pena J, et al. (2009) The PTEN-regulating microRNA miR-26a is amplified in high-grade glioma and facilitates gliomagenesis in vivo. Genes Dev 23: 1327-1337.
37. Weber GL, Parat MO, Binder ZA, Gallia GL, Riggins GJ, (2011) Abrogation of PIK3CA or PIK3R1 reduces proliferation, migration, and invasion in glioblastoma multiforme cells. Oncotarget 2: 833-849.
38. Vander Heiden MG, Cantley LC, Thompson CB, (2009) Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324: 1029-1033.
39. Fuster MM, Esko JD, (2005) The sweet and sour of cancer: glycans as novel therapeutic targets. Nat Rev Cancer 5: 526-542.
40. Yuan K, Kucik D, Singh RK, Listinsky CM, Listinsky JJ, et al. (2008) Alterations in human breast cancer adhesion-motility in response to changes in cell surface glycoproteins displaying alpha-L-fucose moieties. Int J Oncol 32: 797-807.
41. Hakomori S, (1996) Tumor malignancy defined by aberrant glycosylation and sphingo(glyco)lipid metabolism. Cancer Res 56: 5309-5318.
42. Pochec E, Litynska A, Amoresano A, Casbarra A, (2003) Glycosylation profile of integrin alpha 3 beta 1 changes with melanoma progression. Biochim Biophys Acta 1643: 113-123.
43. Spriggs KA, Bushell M, Willis AE, (2010) Translational regulation of gene expression during conditions of cell stress. Mol Cell 40: 228-237.
44. Lu X, de la Pena L, Barker C, Camphausen K, Tofilon PJ, (2006) Radiation-induced changes in gene expression involve recruitment of existing messenger RNAs to and away from polysomes. Cancer Res 66: 1052-1061.
45. Hu X, Pandolfi PP, Li Y, Koutcher JA, Rosenblum M, et al. (2005) mTOR promotes survival and astrocytic characteristics induced by Pten/AKT signaling in glioblastoma. Neoplasia 7: 356-368.
46. Holland EC, Varmus HE, (1998) Basic fibroblast growth factor induces cell migration and proliferation after glia-specific gene transfer in mice. Proc Natl Acad Sci U S A 95: 1218-1223.
47. Hambardzumyan D, Amankulor NM, Helmy KY, Becher OJ, Holland EC, (2009) Modeling Adult Gliomas Using RCAS/t-va Technology. Transl Oncol 2: 89-95.
48. Hambardzumyan D, Becher OJ, Rosenblum MK, Pandolfi PP, Manova-Todorova K, et al. (2008) PI3K pathway regulates survival of cancer stem cells residing in the perivascular niche following radiation in medulloblastoma in vivo. Genes Dev 22: 436-448.