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The Diverse Roles of RNA-Binding Proteins in Glioma Development

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The mRNA Metabolism in Human Disease

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1157))

Abstract

Post-transcriptional regulation of gene expression is fundamental for all forms of life, as it critically contributes to the composition and quantity of a cell’s proteome. These processes encompass splicing, polyadenylation, mRNA decay, mRNA editing and modification and translation and are modulated by a variety of RNA-binding proteins (RBPs). Alterations affecting RBP expression and activity contribute to the development of different types of cancer. In this chapter, we discuss current research shedding light on the role of different RBPs in gliomas. These studies place RBPs as modulators of critical signaling pathways, establish their relevance as prognostic markers and open doors for new therapeutic strategies.

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Abbreviations

RBPs:

RNA-binding proteins

MS:

Mass spectrometry

UTRs:

Untranslated regions

GBM:

Glioblastoma multiforme or Glioblastoma

hnRNP:

Heterogeneous nuclear ribonucleoproteins

PTBP:

Polypyrimidine-tract-binding protein

ADARs:

Adenosine deaminases that act on RNA

HuR:

Hu antigen R

MSI1:

Musashi1

IGF2BPs/IMPs:

Insulin-like growth factor II mRNA binding proteins

PK:

Pyruvate-kinase

EGFR:

Epidermal growth factor receptor

HK2:

Hexokinase2

GLUT3:

Glucose Transporter 3

IG20:

Insuloma-glucagonoma protein 20

RON:

Recepteur d’Origine Nantais

EMT:

Epithelial-mesenchymal transition

PDCD4:

Programmed cell death protein 4

MMP:

Matrix metalloproteinases

STAT3:

Signal transducer and activator of transcription 3

NPC:

Neuronal precursor cells

RRMs:

RNA recognition motifs

FGFR:

fibroblast growth factor receptor-1, -2

FBN:

fibrilin

CASP2:

caspase 2

ABCC1:

ATP binding cassette subfamily C member 1

RTN4:

Reticulon 4

MARK4:

Microtubule affinity-regulating kinase 4

GluR:

Glutamate receptors

ELAV :

Embryonic lethal abnormal visual

AREs :

AU-rich elements

VEGF:

Vascular endothelial growth factor

SIRT1:

Silent mating type information regulation 2 homolog 1

BCL-2:

B-cell lymphoma 2

ProTα:

Prothymosin α

PCM:

pericentriolar matrix

SCs:

Stem cells

GSCs:

Glioblastoma stem cells

MVD:

microvessel density

DNA-PKcs:

DNA-Protein Kinase Catalytic Subunit

PMAs:

Pilomyxoid astrocytomas

QKI:

Quaking

INF:

Interferon

PI3K/MAPK:

Phosphatidylinositol 3-Kinase/Mitogen-activated Protein Kinase

References

  1. Maier T, Güell M, Serrano L (2009) Correlation of mRNA and protein in complex biological samples. FEBS Lett 583:3966–3973

    Article  CAS  PubMed  Google Scholar 

  2. de Sousa Abreu R, Penalva LO, Marcotte EM, Vogel C (2014) Global signatures of protein and mRNA expression levels. Mol BioSyst 5:1512–1526

    Google Scholar 

  3. Castello A, Fischer B, Eichelbaum K et al (2012) Insights into RNA biology from an atlas of mammalian mRNA-binding proteins. Cell 149:1393–1406

    Article  CAS  PubMed  Google Scholar 

  4. Gerstberger S, Hafner M, Tuschl T (2014) A census of human RNA-binding proteins. Nat Rev Genet 15:829–845

    Article  CAS  PubMed  Google Scholar 

  5. Mitchell SF, Parker R (2014) Principles and properties of eukaryotic mRNPs. Mol Cell 54:547–588

    Article  CAS  PubMed  Google Scholar 

  6. Galante PAF, Sandhu D, Abreu RDS, Gradassi M, Vogel C, De Souza SJ, Penalva LOF (2009) A comprehensive in silico expression analysis of RNA binding proteins in normal and tumor tissue: identification of potential players in tumor formation. RNA Biol 6:426–433

    Article  CAS  PubMed  Google Scholar 

  7. Kechavarzi B, Janga SC (2014) Dissecting the expression landscape of RNA-binding proteins in human cancers. Genome Biol 15:R14

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  8. Wang J, Liu Q, Shyr Y (2015) Dysregulated transcription across diverse cancer types reveals the importance of RNA-binding protein in carcinogenesis. BMC Genomics 16:S5

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. Weller M, Wick W, Aldape K, Brada M, Berger M, Nishikawa R, Rosenthal M, Wen PY, Stupp R (2015) Glioma. Natl Rev 1:1–18

    Google Scholar 

  10. Thakkar JP, Dolecek TA, Horbinski C, Ostrom QT, Lightner DD, Barnholtz-Sloan JS, Villano JL (2014) Epidemiologic and molecular prognostic review of glioblastoma. Cancer Epidemiol Biomark Prev 23:1985–1996

    Article  CAS  Google Scholar 

  11. Ostrom QT, Gittleman H, Farah P, Ondracek A, Chen Y, Wolinsky Y, Stroup NE, Kruchko C, Barnholtz-sloan JS (2013) CBTRUS statistical report: primary brain and central nervous system tumors diagnosed in the United States in 2006–2010. J Neuro-Oncol 15:788–796

    Article  CAS  Google Scholar 

  12. Correa BR, De Araujo PR, Qiao M, Burns SC, Chen C, Schlegel R, Agarwal S, Galante PAF, Penalva LOF (2016) Functional genomics analyses of RNA-binding proteins reveal the splicing regulator SNRPB as an oncogenic candidate in glioblastoma. Genome Biol 17:1–16

    Article  CAS  Google Scholar 

  13. Han N, Li W, Zhang M (2013) The function of the RNA-binding protein hnRNP in cancer metastasis. J Cancer Res Ther 9:129–134

    Article  Google Scholar 

  14. Deng J, Chen S, Wang F, Zhao H (2016) Effects of hnRNP A2/B1 knockdown on inhibition of glioblastoma cell invasion, growth and survival. Mol Neurobiol 53:1132–1144

    Article  CAS  PubMed  Google Scholar 

  15. Sueoka E, Sueoka N, Iwanaga K, Sato A, Suga K, Hayashi S, Nagasawa K, Nakachi K (2005) Detection of plasma hnRNP B1 mRNA, a new cancer biomarker, in lung cancer patients by quantitative real-time polymerase chain reaction. Lung Cancer 48:77–83

    Article  PubMed  Google Scholar 

  16. Chen S, Zhang J, Duan L, Zhang Y, Li C, Liu D, Ouyang C, Lu F, Liu X (2014) Identification of HnRNP M as a novel biomarker for colorectal carcinoma by quantitative proteomics. Am J Physiol Gastrointest Liver Physiol 306:394–403

    Article  CAS  Google Scholar 

  17. Loh TJ, Moon H, Cho S et al (2015) CD44 alternative splicing and hnRNP A1 expression are associated with the metastasis of breast cancer. Oncol Rep 34:1231–1238

    Article  CAS  PubMed  Google Scholar 

  18. Noguchi T, Yamada K, Inoue H, Matsuda T, Tanaka T (1987) The L- and R-type isozymes of rat pyruvate kinase are produced from a single gene by use of different promoters. J Biol Chem 262:14366–14371

    CAS  PubMed  Google Scholar 

  19. Noguchi T, Inoue H, Tanaka T (1986) The M1- and M2-type isozymes of rat pyruvate kinase are produced from the same gene by alternative RNA splicing. J Biol Chem 261:13807–13812

    CAS  PubMed  Google Scholar 

  20. David CJ, Chen M, Assanah M, Canoll P, Manley JL (2010) HnRNP proteins controlled by c-Myc deregulate pyruvate kinase mRNA splicing in cancer. Nature 463:364–368

    Article  CAS  PubMed  Google Scholar 

  21. Clower CV, Chatterjee D, Wang Z, Cantley LC (2010) The alternative splicing repressors hnRNP A1/A2 and PTB influence pyruvate kinase isoform expression and cell metabolism. Proc Natl Acad Sci U S A 107:10–15

    Article  Google Scholar 

  22. Parsons DW, Jones S, Zhang X et al (2008) An integrated genomic analysis of human glioblastoma multifome. Science 321:1807–1813

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Guo D, Hildebrandt IJ, Prins RM et al (2009) The AMPK agonist AICAR inhibits the growth of EGFRvIII-expressing glioblastomas by inhibiting lipogenesis. Proc Natl Acad Sci 106:12932–12937

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Babic I, Anderson ES, Tanaka K et al (2013) EGFR mutation-induced alternative splicing of max contributes to growth of glycolytic tumors in brain cancer. Cell Metab 17:1000–1008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Hanahan D, Weinberg RA, Francisco S (2000) The hallmarks of cancer. Cell 100:57–70

    Article  CAS  PubMed  Google Scholar 

  26. Efimova EV, Al-zoubi AM, Martinez O, Kaithamana S, Lu S, Arima T, Prabhakar BS (2004) IG20, in contrast to DENN-SV, (MADD splice variants) suppresses tumor cell survival, and enhances their susceptibility to apoptosis and cancer drugs. Oncogene 23:1076–1087

    Article  CAS  PubMed  Google Scholar 

  27. Prabhakar BS, Mulherkar N, Prasad KV (2008) Role of IG20 splice variants inTRAIL resistance. Mol Pathways 14:347–352

    CAS  Google Scholar 

  28. Ghigna C, Giordano S, Shen H, Benvenuto F, Castiglioni F, Comoglio PM, Green MR, Riva S, Biamonti G, Ferrata V (2005) Cell motility is controlled by SF2/ASF through alternative splicing of the Ron protooncogene. Mol Cell 20:881–890

    Article  CAS  PubMed  Google Scholar 

  29. Lefave CV, Squatrito M, Vorlova S, Rocco GL, Brennan CW, Holland EC, Pan Y, Cartegni L (2011) Splicing factor hnRNPH drives an oncogenic splicing switch in gliomas. EMBO J 30:4084–4097

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Park YM, Hwang J, Masuda K, Choi K, Jeong M, Nam D, Gorospe M (2012) Heterogeneous nuclear ribonucleoprotein C1/C2 controls the metastatic potential of glioblastoma by regulating PDCD4. Mol Cell Biol 32:4237–4244

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Ling JP, Chhabra R, Merran JD, Paul M, Wheelan SJ, Jeffry L, Wong PC (2016) PTBP1 and PTBP2 repress nonconserved cryptic exons. Cell Rep 17:104–113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Romanelli MG, Diani E, Lievens PM-J (2013) New insights into functional roles of the polypyrimidine tract-binding protein. Int J Mol Sci 14:22906–22932

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Boutz PL, Stoilov P, Li Q, Lin C, Chawla G, Ostrow K, Shiue L, Jr MA, Black DL (2007) A post-transcriptional regulatory switch in polypyrimidine tract-binding proteins reprograms alternative splicing in developing neurons. Genes Dev 21:1636–1652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Yamamoto H, Tsukahara K, Kanaoka Y, Jinno S (1999) Isolation of a mammalian homologue of a fission yeast differentiation regulator. Mol Cell Biol 19:3829–3841

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Garcia-Blanco MA, Jamison SF, Sharp PA (1989) Identification and purification of a 62,000-Dalton protein that binds specifically to the polypyrimidine tract of introns. Genes Dev 3:1874–1886

    Article  CAS  PubMed  Google Scholar 

  36. Sawicka K, Bushell M, Spriggs KA, Willis AE (2008) Polypyrimidine-tract-binding protein: a multifunctional RNA-binding protein. Biochem Soc Trans 36:641–647

    Article  CAS  PubMed  Google Scholar 

  37. Cheung HC, Hai T, Zhu W, Baggerly KA, Tsavachidis S, Krahe R, Cote GJ (2009) Splicing factors PTBP1 and PTBP2 promote proliferation and migration of glioma cell lines. Brain J Neurol 132:2277–2288

    Article  Google Scholar 

  38. Cheung HC, Corley LJ, Fuller GN, Mccutcheon IE, Cote GJ (2006) Polypyrimidine tract binding protein and Notch1 are independently re-expressed in glioma. Mod Pathol 19:1034–1041

    Article  CAS  PubMed  Google Scholar 

  39. Schwab JM, Tuli SK, Failli V (2006) The Nogo receptor complex: confining molecules to molecular mechanisms. Trends Mol Med 12:293–297

    Article  CAS  PubMed  Google Scholar 

  40. Oertle T, Huber C, van der Putten H, Schwab M (2003) Genomic structure and functional characterisation of the promoters of human and mouse Nogo/Rtn-4. J Mol Biol 325:299–323

    Article  CAS  PubMed  Google Scholar 

  41. Jin W, Mccutcheon IE, Fuller GN, Huang ES, Cote GJ (2000) Fibroblast growth factor receptor-1 a-exon exclusion and polypyrimidine tract- binding protein in glioblastoma multiforme tumors. Cancer Res 60:1221–1224

    CAS  PubMed  Google Scholar 

  42. Yamaguchi F, Saya H, Bruner JM, Morrison R (1994) Differential expression of two fibroblast growth factor-receptor genes is associated with malignant progression in human astrocytomas. Proc Natl Acad Sci 91:484–488

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Marx A, Nugoor C, Panneerselvam S, Mandelkow E (2010) Structure and function of polarity-inducing kinase family MARK/Par-1 within the branch of AMPK /Snf1-related kinases. FASEB J 24:1637–1648

    Article  CAS  PubMed  Google Scholar 

  44. Moroni RF, Biasi SDE, Colapietro P, Larizza L, Beghini A (2006) Distinct expression pattern of microtubule-associated protein/microtubule affinity-regulating kinase 4 in differentiated neurons. Neuroscience 143:83–94

    Article  CAS  PubMed  Google Scholar 

  45. Fontana L, Rovina D, Novielli C, Maffioli E, Tedeschi G, Magnani I (2015) Suggestive evidence on the involvement of polypyrimidine-tract binding protein in regulating alternative splicing of MAP/microtubule affinity-regulating kinase 4 in glioma. Cancer Lett 359:87–96

    Article  CAS  PubMed  Google Scholar 

  46. Farajollahi S, Maas S (2010) Molecular diversity through RNA editing: a balancing act. Trends Genet 26:221–230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Cenci C, Barzotti R, Galeano F, Corbelli S, Rota R, Massimi L, Di Rocco C, Connell MAO, Gallo A (2008) Down-regulation of RNA editing in pediatric astrocytomas. ADAR2 editing activity inhibits cell migration and proliferaron. J Biol Chem 283:7251–7260

    Article  CAS  PubMed  Google Scholar 

  48. Fu YAO, Zhao X, Li Z, Wei JUN, Tian YU (2016) Splicing variants of ADAR2 and ADAR2-mediated RNA editing in glioma (review). Oncol Lett 12:788–792

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Galeano F, Rossetti C, Tomaselli S, Cifaldi L, Lezzerini M, Pezzullo M, Boldrini R, Massimi L, Di Rocco CM (2012) ADAR2-editing activity inhibits glioblastoma growth through the modulation of the CDC14B/Skp2/p21/p27 axis. Oncogene 32:998–1009

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  50. Brusa R, Zimmermann F, Koh D, Feldmeyer D, Gass P, Seeburg PH, Sprengel R (1995) Early-onset epilepsy and postnatal lethality associated with an editing-deficient GluR-8 allele in mice. Science 270:1677–1680

    Article  CAS  PubMed  Google Scholar 

  51. Maas S, Patt S, Schrey M, Rich A (2001) Underediting of glutamate receptor GluR-B mRNA in malignant gliomas. Neurobiology 98:14687–14692

    CAS  Google Scholar 

  52. Wei J, Li Z, Du C et al (2014) Abnormal expression of an ADAR2 alternative splicing variant in gliomas downregulates adenosine-to-inosine RNA editing. Acta Neurochir 156:1135–1142

    Article  PubMed  Google Scholar 

  53. Li Z, Tian Y, Tian N, Zhao X, Du C, Han L, Zhang H (2015) Aberrant alternative splicing pattern of ADAR2 downregulates adenosine-to-inosine editing in glioma. Oncol Rep 33:2845–2852

    Article  CAS  PubMed  Google Scholar 

  54. Tomaselli S, Galeano F, Alon S et al (2015) Modulation of microRNA editing, expression and processing by ADAR2 deaminase in glioblastoma. Genome Biol 16:5

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  55. Srikantan S, Gorospe M (2015) HuR function in disease. Front Biosci 17:189–205

    Article  Google Scholar 

  56. Hinman MN, Lou H (2008) Diverse molecular functions of Hu proteins. Cell Mol Life Sci 65:3168–3181

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Gurgis FMS, Yeung YT, Tang MXM, Heng B, Buckland M, Ammit AJ, Haapasalo J, Haapasalo H, Guillemin GJ, Grewal T (2015) The p38-MK2-HuR pathway potentiates EGFRvIII-IL-1β-driven IL-6 secretion in glioblastoma cells. Oncogene 34:2934–2942

    Article  CAS  PubMed  Google Scholar 

  58. Wang W, Caldwell MC, Lin S, Furneaux H, Gorospe M (2000) HuR regulates cyclin A and cyclin B1 mRNA stability during cell proliferation. EMBO J 19:2340–2350

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Ido K, Nakagawa T, Sakuma T, Takeuchi H, Sato K (2008) Expression of vascular endothelial growth factor-A and mRNA stability factor HuR in human astrocytic tumors. Neuropathology 28:604–611

    PubMed  Google Scholar 

  60. Abdelmohsen K, Gorospe M (2007) Posttranscriptional orchestration of an anti-apoptotic program by HuR. Cell Cycle 6:1288–1292

    Article  CAS  PubMed  Google Scholar 

  61. López de Silanes I, Zhan M, Lal A, Yang X, Gorospe M (2004) Identification of a target RNA motif for RNA-binding protein HuR. Proc Natl Acad Sci U S A 101:2987–2992

    Article  PubMed  CAS  Google Scholar 

  62. Uren PJ, Burns SC, Ruan J, Singh KK, Smith AD, Penalva LOF (2011) Genomic analyses of the RNA-binding protein hu antigen R (HuR) identify a complex network of target genes and novel characteristics of its binding sites. J Biol Chem 286:37063–37066

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Mukherjee K, Ghoshal B, Ghosh S, Chakrabarty Y, Das S, Bhattacharyya SN (2016) Reversible HuR-microRNA binding controls extracellular export of miR-122 and augments stress response. EMBO Rep 17:1184–1203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Young LE, Moore AE, Sokol L, Meisner-kober N, Dixon DA (2012) The mRNA stability factor HuR inhibits MicroRNA-16 targeting of cyclooxygenase-2. Mol Cancer Res 10:167–180

    Article  CAS  PubMed  Google Scholar 

  65. Goldberg-cohen I, Furneauxb H, Levy AP (2002) A 40-bp RNA element that mediates stabilization of vascular endothelial growth factor mRNA by HuR. J Biol Chem 277:13635–13640

    Article  CAS  PubMed  Google Scholar 

  66. Bolognani F, Gallani A-I, Sokol L, Baskin DS, Meisner-Kober N (2012) mRNA stability alterations mediated by HuR are necessary to sustain the fast growth of glioma cells. J Neuro-Oncol 106:531–542

    Article  CAS  Google Scholar 

  67. Nabors LB, Gillespie GY, Harkins L, King PH (2001) HuR, a RNA stability factor, is expressed in malignant brain tumors and binds to adenine- and uridine-rich elements within the 3′ untranslated regions of cytokine and angiogenic factor mRNAs. Cancer Res 61:2154–2161

    CAS  PubMed  Google Scholar 

  68. Filippova N, Yang X, Wang Y, Gillespie GY, Langford C (2011) The RNA-binding protein HuR promotes glioma growth and treatment resistance. Mol Cancer Res 9:648–660

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Yeung YT, Mcdonald KL, Grewal T, Munoz L (2013) Interleukins in glioblastoma pathophysiology: implications for therapy. Br J Pharmacol 168:591–606

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Filippova N, Yang X, King P, Nabors LB (2012) Phosphoregulation of the RNA-binding protein Hu antigen R (HuR) by Cdk5 affects centrosome function. J Biol Chem 287:32277–32287

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. De Boer L, Oakes V, Beamish H, Giles N, Stevens F, Desouza C (2008) Cyclin A/cdk2 coordinates centrosomal and nuclear mitotic events. Oncogene 27:4261–4268

    Article  PubMed  CAS  Google Scholar 

  72. Filippova N, Yang X, Nabors LB (2015) Growth factor dependent regulation of centrosome function and genomic instability by HuR. Biomol Ther 5:263–281

    CAS  Google Scholar 

  73. Mukherjee J, Ohba S, See WL, Phillips JJ, Molinaro AM, Pieper RO (2016) PKM2 uses control of HuR localization to regulate p27 and cell cycle progression in human glioblastoma cells. Int J Cancer 139:99–111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Holmes B, Benavides-Serrato A, Freeman RS, Landon KA, Bashir T, Nishimura RN, Gera J (2017) mTORC2/AKT/HSF1/HuR constitute a feed-forward loop regulating Rictor expression and tumor growth in glioblastoma. Oncogene 37:732–743

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  75. Yang W, Yu H, Shen Y, Liu Y, Yang Z (2016) MiR-146b-5p overexpression attenuates stemness and radioresistance of glioma stem cells by targeting HuR/lincRNA-p21/β-catenin pathway. Oncotarget 7:41505–41526

    PubMed  PubMed Central  Google Scholar 

  76. Okano H, Kawahara H, Toriya M, Nakao K, Shibata S, Imai T (2005) Function of RNA-binding protein Musashi-1 in stem cells. Exp Cell Res 306:349–356

    Article  CAS  PubMed  Google Scholar 

  77. Kudinov AE, Karanicolas J, Golemis EA, Boumber Y (2017) Musashi RNA-binding proteins as cancer drivers and novel therapeutic targets. Clin Cancer Res 23:2143–2154

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Shu H-J, Saito T, Watanabe H, Ito J-I, Takeda H, Okano H, Kawata S (2002) Expression of the Musashi1 gene encoding the RNA-binding protein in human hepatoma cell lines. Biochem Biophys Res Commun 293:150–154

    Article  CAS  PubMed  Google Scholar 

  79. Ye F, Zhou C, Cheng Q, Shen J, Chen H (2008) Stem-cell-abundant proteins nanog, nucleostemin and Musashi1 are highly expressed in malignant cervical epithelial cells. BMC Cancer 8:108

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  80. Wang X-Y, Penalva LO, Yuan H, Linnoila RI, Lu J, Okano H, Glazer RI (2010) Musashi1 regulates breast tumor cell proliferation and is a prognostic indicator of poor survival. Mol Cancer 9:221

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  81. Dahlrot RH, Hansen S, Hjelmborg J, Kristensen BW (2013) Prognostic value of Musashi-1 in gliomas. J Neuro-Oncol 115:453–461

    Article  CAS  Google Scholar 

  82. Vo DT, Subramaniam D, Remke M et al (2012) The RNA-binding protein Musashi1 affects medulloblastoma growth via a network of cancer- related genes and is an indicator of poor prognosis. Am J Pathol 181:1762–1772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Uren PJ, Vo DT, De Araujo R et al (2015) RNA-binding protein Musashi1 is a central regulator of adhesion pathways in glioblastoma. Mol Cell Biol 35:2965–2978

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. de Araujo PR, Grothi A, da Silva AE, Tonapi SS, Burns SC, Qiao M, Uren PJ, Yuan Z-M, Bishop AJR, Penalva LOF (2016) Musashi1 impacts radio-resistance in glioblastoma by controlling DNA-protein kinase catalytic subunit. Am J Pathol 186:2271–2278

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  85. Chen H, Lin L, Wang M et al (2016) Musashi-1 regulates AKT-derived IL-6 autocrinal/paracrinal malignancy and chemoresistance in glioblastoma. Oncotarget 7:42485–42501

    PubMed  PubMed Central  Google Scholar 

  86. Nielsen J, Christiansen JAN, Lykke-andersen J, Johnsen AH, Wewer UM, Nielsen FC (1999) A family of insulin-like growth factor II mRNA-binding proteins represses translation in late development. Mol Cell Biol 19:1262–1270

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Degrauwe N, Suvà M, Janiszewska M, Riggi N, Stamenkovic I (2016) IMPs: an RNA-binding protein family that provides a link between stem cell maintenance in normal development and cancer. Genes Dev 30:2459–2474

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Suvasini R, Shruti B, Thota B et al (2011) Insulin growth factor-2 binding protein 3 (IGF2BP3) is a glioblastoma-specific marker that activates phosphatidylinositol 3-kinase/mitogen-activated protein kinase (PI3K/MAPK) pathways by modulating IGF-2. J Biol Chem 286:25882–25890

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Barton VN, Donson AM, Birks DK, Kleinschmidt-demasters BK, Handler MH, Foreman NK, Rush SZ (2013) Insulin-like growth factor 2 mRNA binding protein 3 expression is an independent prognostic factor in pediatric pilocytic and pilomyxoid astrocytoma. J Neuropathol Exp Neurol 72:442–449

    Article  CAS  PubMed  Google Scholar 

  90. Serão NVL, Delfino KR, Southey BR, Beever JE, Rodriguez-zas SL (2011) Cell cycle and aging, morphogenesis, and response to stimuli genes are individualized biomarkers of glioblastoma progression and survival. BMC Med Genet 4:49

    Google Scholar 

  91. Shu C, Wang Q, Yan X, Wang J (2018) Whole-genome expression microarray combined with machine learning to identify prognostic biomarkers for high-grade glioma. J Mol Neurosci 64:491–500

    Article  CAS  PubMed  Google Scholar 

  92. Degrauwe N, Schlumpf TB, Janiszewska M, Martin P, Cauderay A, Provero P, Riggi N, Suvà M, Paro R, Stamenkovic I (2016) The RNA binding protein IMP2 preserves glioblastoma stem cells by preventing let-7 target gene silencing. Cell Rep 15:1634–1647

    Article  CAS  PubMed  Google Scholar 

  93. Darbelli L, Richard S (2016) Emerging functions of the quaking RNA-binding proteins and link to human diseases. Wiley Interdiscip Rev RNA 7:399–412

    Article  CAS  PubMed  Google Scholar 

  94. Li ZZ, Kondo T, Murata T, Ebersole TA, Nishi T, Ushio Y, Yamamura K, Abe K (2002) Expression of Hqk encoding a KH RNA binding protein is altered in human glioma. Jpn J Cancer Res 93:167–177

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Jiang L, Saetre P, Radomska KJ, Jazin E, Carlstrom EL (2010) QKI-7 regulates expression of interferon-related genes in human astrocyte glioma cells. PLoS One 5:e13079

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  96. Xi Z, Wang P, Xue Y, Shang C, Liu X, Ma J, Li Z, Li Z, Bao M, Liu Y (2017) Overexpression of miR-29a reduces the oncogenic properties of glioblastoma stem cells by downregulating quaking gene isoform 6. Oncotarget 8:24949–24963

    PubMed  PubMed Central  Google Scholar 

  97. Bandopadhayay P, Ramkissoon LA, Jain P et al (2016) MYB-QKI rearrangements in angiocentric glioma drive tumorigenicity through a tripartite mechanism. Nat Genet 48:273–282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Aronco LD, Rouleau C, Gayden T, Crevier L, Claude J, Sébastien D, Nada P, Bandopadhayay P, Ligon KL, Ellezam B (2017) Brainstem angiocentric gliomas with MYB – QKI rearrangements. Acta Neuropathol 134:667–669

    Article  PubMed  PubMed Central  Google Scholar 

  99. Chan E, Bollen AW, Sirohi D, Van Ziffle J, Grenert JP, Kline CN, Tihan T, Perry A, Gupta N, Solomon DA (2017) Angiocentric glioma with MYB-QKI fusion located in the brainstem, rather than cerebral cortex. Acta Neuropathol 134:671–673

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

Mitzli X. Velasco belongs to the “Programa de Doctorado en Ciencias Biomédicas, Facultad de Medicina, Universidad Nacional Autónoma de México, CONACYT. No. de becario 270268”.

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Authors and Affiliations

  1. Laboratory of Translation and Cancer, Unit of Biomedical Research on Cancer, Instituto Nacional de Cancerología (INCan), Mexico City, Mexico

    Mitzli X. Velasco & Greco Hernández

  2. Biomedical Sciences Ph.D. Program, National Autonomous University of Mexico, UNAM, Mexico City, Mexico

    Mitzli X. Velasco

  3. Greehey Children’s Cancer Research Institute, University of Texas Health Science Center at San Antonio, San Antonio, TX, USA

    Mitzli X. Velasco, Adam Kosti & Luiz O. F. Penalva

Authors
  1. Mitzli X. Velasco
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  2. Adam Kosti
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  3. Luiz O. F. Penalva
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  4. Greco Hernández
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Corresponding authors

Correspondence to Luiz O. F. Penalva or Greco Hernández .

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Editors and Affiliations

  1. Department of Human Genetics, National Institute of Health Doutor Ricardo Jorge, Lisboa, Portugal, Faculty of Sciences, BioISI – Biosystems & Integrative Sciences Institute, University of Lisbon, Lisboa, Portugal

    Luísa Romão

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Velasco, M.X., Kosti, A., Penalva, L.O.F., Hernández, G. (2019). The Diverse Roles of RNA-Binding Proteins in Glioma Development. In: Romão, L. (eds) The mRNA Metabolism in Human Disease. Advances in Experimental Medicine and Biology, vol 1157. Springer, Cham. https://doi.org/10.1007/978-3-030-19966-1_2

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