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The master regulator FUBP1: its emerging role in normal cell function and malignant development

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Abstract

The human Far Upstream Element (FUSE) Binding Protein 1 (FUBP1) is a multifunctional DNA- and RNA-binding protein involved in diverse cellular processes. FUBP1 is a master regulator of transcription, translation, and RNA splicing. FUBP1 has been identified as a potent pro-proliferative and anti-apoptotic factor by modulation of complex networks. FUBP1 is also described either as an oncoprotein or a tumor suppressor. Especially, FUBP1 overexpression is observed in a growing number of cancer and leads to a deregulation of targets that includes the fine-tuned MYC oncogene. Moreover, recent loss-of-function analyses of FUBP1 establish its essential functions in hematopoietic stem cell maintenance and survival. Therefore, FUBP1 appears as an emerging suspect in hematologic disorders in addition to solid tumors. The scope of the present review is to describe the advances in our understanding of the molecular basis of FUBP1 functions in normal cells and carcinogenesis. We also delineate the recent progresses in the understanding of the master role of FUBP1 in normal and pathological hematopoiesis. We conclude that FUBP1 is not only worth studying biologically but is also of clinical relevance through its pivotal role in regulating multiple cellular processes and its involvement in oncogenesis.

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Abbreviations

ALL:

Acute lymphoblastic leukemia

AML:

Acute myeloid leukemia

ARE:

AU-rich elements

CCRCC:

Clear cell renal cell carcinoma

ChIP:

Chromatin immunoprecipitation

CLL:

Chronic lymphocytic leukemia

EMSA:

Electrophoretic mobility shift assay

EV71:

Enterovirus 71

FACS:

Fluorescence activated cell sorting

FDA:

Food and drug administration

HCC:

Hepatocellular carcinoma

HCV:

Hepatitis C virus

HSC:

Hematopoietic stem cells

IRES:

Internal ribosome entry site

KO:

Knock-out

NLS:

Nuclear localization signal

NSCLC:

Non-small cell lung cancer

SELEX:

Systematic evolution of ligands by exponential enrichment

SNV:

Single nucleotide variation

ssDNA:

Single-stranded DNA

TSS:

Transcription start site

References

  1. Zhang J, Chen QM (2013) Far upstream element binding protein 1: a commander of transcription, translation and beyond. Oncogene 32:2907–2916

    Article  CAS  PubMed  Google Scholar 

  2. Avigan MI, Strober B, Levens D (1990) A far upstream element stimulates c-myc expression in undifferentiated leukemia cells. J Biol Chem 265:18538–18545

    CAS  PubMed  Google Scholar 

  3. Duncan R, Bazar L, Michelotti G et al (1994) A sequence-specific, single-strand binding protein activates the far upstream element of c-myc and defines a new DNA-binding motif. Genes Dev 8:465–480. https://doi.org/10.1101/gad.8.4.465

    Article  CAS  PubMed  Google Scholar 

  4. Levens D (2008) How the c-myc promoter works and why it sometimes does not. JNCI Monogr 2008:41–43. https://doi.org/10.1093/jncimonographs/lgn004

    Article  CAS  Google Scholar 

  5. Liu J, Chung H-J, Vogt M et al (2011) JTV1 co-activates FBP to induce USP29 transcription and stabilize p53 in response to oxidative stress. EMBO J 30:846–858. https://doi.org/10.1038/emboj.2011.11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Malz M, Weber A, Singer S et al (2009) Overexpression of far upstream element binding proteins: a mechanism regulating proliferation and migration in liver cancer cells. Hepatology 50:1130–1139. https://doi.org/10.1002/hep.23051

    Article  CAS  PubMed  Google Scholar 

  7. Malz M, Bovet M, Samarin J et al (2014) Overexpression of far upstream element (FUSE) binding protein (FBP)-interacting repressor (FIR) supports growth of hepatocellular carcinoma. Hepatology 60:1241–1250

    Article  CAS  PubMed  Google Scholar 

  8. Rabenhorst U, Beinoraviciute-Kellner R, Brezniceanu M-L et al (2009) Overexpression of the far upstream element binding protein 1 in hepatocellular carcinoma is required for tumor growth. Hepatology 50:1121–1129. https://doi.org/10.1002/hep.23098

    Article  CAS  PubMed  Google Scholar 

  9. Baumgarten P, Harter PN, Tönjes M et al (2014) Loss of FUBP1 expression in gliomas predicts FUBP1 mutation and is associated with oligodendroglial differentiation, IDH1 mutation and 1p/19q loss of heterozygosity: FUBP1 expression in human gliomas. Neuropathol Appl Neurobiol 40:205–216. https://doi.org/10.1111/nan.12088

    Article  CAS  PubMed  Google Scholar 

  10. Duan J, Bao X, Ma X et al (2017) Upregulation of far upstream element-binding protein 1 (FUBP1) promotes tumor proliferation and tumorigenesis of clear cell renal cell carcinoma. PLoS One 12:e0169852. https://doi.org/10.1371/journal.pone.0169852

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Hauck S, Hiesinger K, Khageh Hosseini S et al (2016) Pyrazolo[1,5a]pyrimidines as a new class of FUSE binding protein 1 (FUBP1) inhibitors. Bioorg Med Chem 24:5717–5729. https://doi.org/10.1016/j.bmc.2016.09.015

    Article  CAS  PubMed  Google Scholar 

  12. Singer S, Malz M, Herpel E et al (2009) Coordinated expression of stathmin family members by far upstream sequence element-binding protein-1 increases motility in non-small cell lung cancer. Cancer Res 69:2234–2243. https://doi.org/10.1158/0008-5472.CAN-08-3338

    Article  CAS  PubMed  Google Scholar 

  13. Bettegowda C, Agrawal N, Jiao Y et al (2011) Mutations in CIC and FUBP1 contribute to human oligodendroglioma. Science 333:1453–1455. https://doi.org/10.1126/science.1210557

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Yang L, Zhu J, Zhang J et al (2016) Far upstream element-binding protein 1 (FUBP1) is a potential c-Myc regulator in esophageal squamous cell carcinoma (ESCC) and its expression promotes ESCC progression. Tumor Biol 37:4115–4126. https://doi.org/10.1007/s13277-015-4263-8

    Article  CAS  Google Scholar 

  15. Ding Z, Liu X, Liu Y et al (2015) Expression of far upstream element (FUSE) binding protein 1 in human glioma is correlated with c-Myc and cell proliferation. Mol Carcinog 54:405–415. https://doi.org/10.1002/mc.22114

    Article  CAS  PubMed  Google Scholar 

  16. Rabenhorst U, Thalheimer FB, Gerlach K et al (2015) Single-stranded DNA-binding transcriptional regulator FUBP1 is essential for fetal and adult hematopoietic stem cell self-renewal. Cell Rep 11:1847–1855. https://doi.org/10.1016/j.celrep.2015.05.038

    Article  CAS  PubMed  Google Scholar 

  17. Zhou W, Chung Y-J, Castellar ER et al (2016) Far upstream element binding protein plays a crucial role in embryonic development, hematopoiesis, and stabilizing MYC expression levels. Am J Pathol. https://doi.org/10.1016/j.ajpath.2015.10.028

    Article  PubMed  PubMed Central  Google Scholar 

  18. Duncan R, Collins I, Tomonaga T et al (1996) A unique transactivation sequence motif is found in the carboxyl-terminal domain of the single-strand-binding protein FBP. Mol Cell Biol 16:2274–2282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Davis-Smyth T, Duncan RC, Zheng T et al (1996) The far upstream element-binding proteins comprise an ancient family of single-strand DNA-binding transactivators. J Biol Chem 271:31679–31687. https://doi.org/10.1074/jbc.271.49.31679

    Article  CAS  PubMed  Google Scholar 

  20. Chung H-J, Liu J, Dundr M et al (2006) FBPs are calibrated molecular tools to adjust gene expression. Mol Cell Biol 26:6584–6597. https://doi.org/10.1128/MCB.00754-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Briata P, Bordo D, Puppo M et al (2016) Diverse roles of the nucleic acid-binding protein KHSRP in cell differentiation and disease. Wiley Interdiscip Rev RNA 7:227–240. https://doi.org/10.1002/wrna.1327

    Article  CAS  PubMed  Google Scholar 

  22. Gherzi R, Lee K-Y, Briata P et al (2004) A KH domain RNA binding protein, KSRP, promotes ARE-directed mRNA turnover by recruiting the degradation machinery. Mol Cell 14:571–583. https://doi.org/10.1016/j.molcel.2004.05.002

    Article  CAS  PubMed  Google Scholar 

  23. Gau B-H, Chen T-M, Shih Y-HJ, Sun HS (2011) FUBP3 interacts with FGF9 3′ microsatellite and positively regulates FGF9 translation. Nucleic Acids Res 39:3582–3593. https://doi.org/10.1093/nar/gkq1295

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Weber A, Kristiansen I, Johannsen M et al (2008) The FUSE binding proteins FBP1 and FBP3 are potential c-myc regulators in renal, but not in prostate and bladder cancer. BMC Cancer 8:369. https://doi.org/10.1186/1471-2407-8-369

    Article  PubMed  PubMed Central  Google Scholar 

  25. Zerbino DR, Achuthan P, Akanni W et al (2018) Ensembl 2018. Nucleic Acids Res 46:D754–D761. https://doi.org/10.1093/nar/gkx1098

    Article  CAS  PubMed  Google Scholar 

  26. Rebhan M, Chalifa-Caspi V, Prilusky J, Lancet D (1997) GeneCards: integrating information about genes, proteins and diseases. Trends Genet TIG 13:163

    Article  CAS  PubMed  Google Scholar 

  27. Valverde R, Edwards L, Regan L (2008) Structure and function of KH domains: structure and function of KH domains. FEBS J 275:2712–2726. https://doi.org/10.1111/j.1742-4658.2008.06411.x

    Article  CAS  PubMed  Google Scholar 

  28. Chien H-L, Liao C-L, Lin Y-L (2011) FUSE binding protein 1 interacts with untranslated regions of japanese encephalitis virus RNA and negatively regulates viral replication. J Virol 85:4698–4706. https://doi.org/10.1128/JVI.01950-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Tang Q, Xia W, Ji Q et al (2014) Role of far upstream element binding protein 1 in colonic epithelial disruption during dextran sulphate sodium-induced murine colitis. Int J Clin Exp Pathol 7:2019–2031

    PubMed  PubMed Central  Google Scholar 

  30. Jang M, Park BC, Kang S et al (2009) Far upstream element-binding protein-1, a novel caspase substrate, acts as a cross-talker between apoptosis and the c-myc oncogene. Oncogene 28:1529–1536

    Article  CAS  PubMed  Google Scholar 

  31. Kim MJ, Park B-J, Kang Y-S et al (2003) Downregulation of FUSE-binding protein and c-myc by tRNA synthetase cofactor p38 is required for lung cell differentiation. Nat Genet 34:330–336. https://doi.org/10.1038/ng1182

    Article  CAS  PubMed  Google Scholar 

  32. Atanassov BS, Dent SYR (2011) USP22 regulates cell proliferation by deubiquitinating the transcriptional regulator FBP1. EMBO Rep 12:924–930. https://doi.org/10.1038/embor.2011.140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Hornbeck PV, Zhang B, Murray B et al (2015) PhosphoSitePlus, 2014: mutations, PTMs and recalibrations. Nucleic Acids Res 43:D512–D520. https://doi.org/10.1093/nar/gku1267

    Article  CAS  PubMed  Google Scholar 

  34. Venturutti L, Cordo Russo RI, Rivas MA et al (2016) MiR-16 mediates trastuzumab and lapatinib response in ErbB-2-positive breast and gastric cancer via its novel targets CCNJ and FUBP1. Oncogene 35:6189–6202. https://doi.org/10.1038/onc.2016.151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Zhao D, Zhang Y, Song L (2017) MiR-16-1 targeted silences far upstream element binding protein 1 to advance the chemosensitivity to adriamycin in gastric cancer. Pathol Oncol Res POR. https://doi.org/10.1007/s12253-017-0263-x

    Article  PubMed  Google Scholar 

  36. Marceau AH (2012) Functions of single-strand DNA-binding proteins in DNA replication, recombination, and repair. Methods Mol Biol Clifton NJ 922:1–21. https://doi.org/10.1007/978-1-62703-032-8_1

    Article  CAS  Google Scholar 

  37. Michelotti GA, Michelotti EF, Pullner A et al (1996) Multiple single-stranded cis elements are associated with activated chromatin of the human c-myc gene in vivo. Mol Cell Biol 16:2656–2669

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Michelotti EF, Michelotti GA, Aronsohn AI, Levens D (1996) Heterogeneous nuclear ribonucleoprotein K is a transcription factor. Mol Cell Biol 16:2350–2360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Tomonaga T, Levens D (1996) Activating transcription from single stranded DNA. Proc Natl Acad Sci USA 93:5830–5835

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Braddock DT (2002) Molecular basis of sequence-specific single-stranded DNA recognition by KH domains: solution structure of a complex between hnRNP K KH3 and single-stranded DNA. EMBO J 21:3476–3485. https://doi.org/10.1093/emboj/cdf352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Braddock DT, Louis JM, Baber JL et al (2002) Structure and dynamics of KH domains from FBP bound to single-stranded DNA. Nature 415:1051–1056. https://doi.org/10.1038/4151051a

    Article  CAS  PubMed  Google Scholar 

  42. Hsiao H, Nath A, Lin C-Y et al (2010) Quantitative characterization of the interactions among c-myc transcriptional regulators FUSE, FBP, and FIR. Biochemistry (Mosc) 49:4620–4634. https://doi.org/10.1021/bi9021445

    Article  CAS  Google Scholar 

  43. Benjamin LR, Chung H-J, Sanford S et al (2008) Hierarchical mechanisms build the DNA-binding specificity of FUSE binding protein. Proc Natl Acad Sci 105:18296–18301

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Debaize L, Jakobczyk H, Avner S et al (2018) Interplay between transcription regulators RUNX1 and FUBP1 activates an enhancer of the oncogene c-KIT and amplifies cell proliferation. Nucleic Acids Res. https://doi.org/10.1093/nar/gky756

    Article  PubMed  PubMed Central  Google Scholar 

  45. Stine ZE, Walton ZE, Altman BJ et al (2015) MYC, metabolism, and cancer. Cancer Discov 5:1024–1039. https://doi.org/10.1158/2159-8290.CD-15-0507

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Dang CV (2012) MYC on the Path to Cancer. Cell 149:22–35. https://doi.org/10.1016/j.cell.2012.03.003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. He L, Liu J, Collins I et al (2000) Loss of FBP function arrests cellular proliferation and extinguishes c-myc expression. EMBO J 19:1034–1044. https://doi.org/10.1093/emboj/19.5.1034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Feaver WJ, Svejstrup JQ, Bardwell L et al (1993) Dual roles of a multiprotein complex from S. cerevisiae in transcription and DNA repair. Cell 75:1379–1387. https://doi.org/10.1016/0092-8674(93)90624-Y

    Article  CAS  PubMed  Google Scholar 

  49. Schaeffer L, Roy R, Humbert S et al (1993) DNA repair helicase: a component of BTF2 (TFIIH) basic transcription factor. Science 260:58–63. https://doi.org/10.1126/science.8465201

    Article  CAS  PubMed  Google Scholar 

  50. Compe E, Egly J-M (2012) TFIIH: when transcription met DNA repair. Nat Rev Mol Cell Biol 13:343. https://doi.org/10.1038/nrm3350

    Article  CAS  PubMed  Google Scholar 

  51. Parvin JD, Sharp PA (1993) DNA topology and a minimal set of basal factors for transcription by RNA polymerase II. Cell 73:533–540

    Article  CAS  PubMed  Google Scholar 

  52. Goodrich JA, Tjian R (1994) Transcription factors IIE and IIH and ATP hydrolysis direct promoter clearance by RNA polymerase II. Cell 77:145–156

    Article  CAS  PubMed  Google Scholar 

  53. Felsher DW, Bishop JM (1999) Transient excess of MYC activity can elicit genomic instability and tumorigenesis. Proc Natl Acad Sci USA 96:3940–3944

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Liu J, He L, Collins I et al (2000) The FBP interacting repressor targets TFIIH to inhibit activated transcription. Mol Cell 5:331–341. https://doi.org/10.1016/S1097-2765(00)80428-1

    Article  CAS  PubMed  Google Scholar 

  55. Liu J, Kouzine F, Nie Z et al (2006) The FUSE/FBP/FIR/TFIIH system is a molecular machine programming a pulse of c-myc expression. EMBO J 25:2119–2130. https://doi.org/10.1038/sj.emboj.7601101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Matsushita K, Tomonaga T, Shimada H et al (2006) An essential role of alternative splicing of c-myc suppressor FUSE-binding protein-interacting repressor in carcinogenesis. Cancer Res 66:1409–1417. https://doi.org/10.1158/0008-5472.CAN-04-4459

    Article  CAS  PubMed  Google Scholar 

  57. Crichlow GV, Zhou H, Hsiao H et al (2008) Dimerization of FIR upon FUSE DNA binding suggests a mechanism of c-myc inhibition. EMBO J 27:277–289. https://doi.org/10.1038/sj.emboj.7601936

    Article  CAS  PubMed  Google Scholar 

  58. Weber A, Liu J, Collins I, Levens D (2005) TFIIH operates through an expanded proximal promoter to fine-tune c-myc expression. Mol Cell Biol 25:147–161. https://doi.org/10.1128/MCB.25.1.147-161.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Rubin CI, Atweh GF (2004) The role of stathmin in the regulation of the cell cycle. J Cell Biochem 93:242–250. https://doi.org/10.1002/jcb.20187

    Article  CAS  PubMed  Google Scholar 

  60. Mistry SJ, Atweh GF (2002) Role of stathmin in the regulation of the mitotic spindle: potential applications in cancer therapy. Mt Sinai J Med N Y 69:299–304

    Google Scholar 

  61. Belletti B, Nicoloso MS, Schiappacassi M et al (2008) Stathmin activity influences sarcoma cell shape, motility, and metastatic potential. Mol Biol Cell 19:2003–2013. https://doi.org/10.1091/mbc.E07-09-0894

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Kuner R, Muley T, Meister M et al (2009) Global gene expression analysis reveals specific patterns of cell junctions in non-small cell lung cancer subtypes. Lung Cancer Amst Neth 63:32–38. https://doi.org/10.1016/j.lungcan.2008.03.033

    Article  Google Scholar 

  63. Krumlauf R (1994) Hox genes in vertebrate development. Cell 78:191–201

    Article  CAS  PubMed  Google Scholar 

  64. Lawrence HJ, Sauvageau G, Humphries RK, Largman C (1996) The role of HOX homeobox genes in normal and leukemic hematopoiesis. Stem Cells Dayt Ohio 14:281–291. https://doi.org/10.1002/stem.140281

    Article  CAS  Google Scholar 

  65. Broudy VC (1997) Stem cell factor and hematopoiesis. Blood 90:1345–1364

    CAS  PubMed  Google Scholar 

  66. Kitamura Y, Hirotab S (2004) Kit as a human oncogenic tyrosine kinase. Cell Mol Life Sci CMLS 61:2924–2931. https://doi.org/10.1007/s00018-004-4273-y

    Article  CAS  PubMed  Google Scholar 

  67. Gartel AL, Serfas MS, Tyner AL (1996) p21–negative regulator of the cell cycle. Proc Soc Exp Biol Med 213:138–149

    Article  CAS  PubMed  Google Scholar 

  68. Gartel AL, Tyner AL (2002) The role of the cyclin-dependent kinase inhibitor p21 in apoptosis. Mol Cancer Ther 1:639–649

    CAS  PubMed  Google Scholar 

  69. Soria G, Speroni J, Podhajcer OL et al (2008) p21 differentially regulates DNA replication and DNA-repair-associated processes after UV irradiation. J Cell Sci 121:3271–3282. https://doi.org/10.1242/jcs.027730

    Article  CAS  PubMed  Google Scholar 

  70. Dixit U, Liu Z, Pandey AK et al (2014) Fuse binding protein antagonizes the transcription activity of tumor suppressor protein. BMC Cancer. https://doi.org/10.1186/1471-2407-14-925

    Article  PubMed  PubMed Central  Google Scholar 

  71. Dixit U, Pandey AK, Liu Z et al (2015) FUSE binding protein 1 facilitates persistent hepatitis C virus replication in hepatoma cells by regulating tumor suppressor p53. J Virol 89:7905–7921. https://doi.org/10.1128/JVI.00729-15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Frost JR, Mendez M, Soriano AM (2018) Adenovirus 5 E1A-mediated suppression of p53 via FUBP1. J Virol. https://doi.org/10.1128/jvi.00439-18

    Article  PubMed  PubMed Central  Google Scholar 

  73. Sully G, Dean JLE, Wait R et al (2004) Structural and functional dissection of a conserved destabilizing element of cyclo-oxygenase-2 mRNA: evidence against the involvement of AUF-1 [AU-rich element/poly(U)-binding/degradation factor-1], AUF-2, tristetraprolin, HuR (Hu antigen R) or FBP1 (far-upstream-sequence-element-binding protein 1). Biochem J 377:629–639. https://doi.org/10.1042/BJ20031484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Zhang Z, Harris D, Pandey VN (2008) The FUSE binding protein is a cellular factor required for efficient replication of hepatitis C virus. J Virol 82:5761–5773. https://doi.org/10.1128/JVI.00064-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Caput D, Beutler B, Hartog K et al (1986) Identification of a common nucleotide sequence in the 3′-untranslated region of mRNA molecules specifying inflammatory mediators. Proc Natl Acad Sci USA 83:1670–1674

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Zhang T, Kruys V, Huez G, Gueydan C (2002) AU-rich element-mediated translational control: complexity and multiple activities of trans-activating factors. Biochem Soc Trans 30:952–958. https://doi.org/10.1042/bst0300952

    Article  CAS  PubMed  Google Scholar 

  77. Roberto Gherzi, Ching-Yi Chen, Michele Trabucchi et al (2010) The role of KSRP in mRNA decay and microRNA precursor maturation. Wiley Interdiscip Rev RNA 1:230–239. https://doi.org/10.1002/wrna.2

    Article  CAS  Google Scholar 

  78. Jacob AG, Singh RK, Mohammad F et al (2014) The splicing factor FUBP1 is required for the efficient splicing of oncogene MDM2 Pre-mRNA. J Biol Chem 289:17350–17364. https://doi.org/10.1074/jbc.M114.554717

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Miro J, Laaref AM, Rofidal V et al (2015) FUBP1: a new protagonist in splicing regulation of the DMD gene. Nucleic Acids Res 43:2378–2389. https://doi.org/10.1093/nar/gkv086

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Zheng W, Shen F, Hu R et al (2016) Far upstream element-binding protein 1 binds the 3′ untranslated region of PKD2 and suppresses its translation. J Am Soc Nephrol. https://doi.org/10.1681/asn.2015070836

    Article  PubMed  PubMed Central  Google Scholar 

  81. Irwin N, Baekelandt V, Goritchenko L, Benowitz LI (1997) Identification of two proteins that bind to a pyrimidine-rich sequence in the 3′-untranslated region of GAP-43 mRNA. Nucleic Acids Res 25:1281–1288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Olanich ME, Moss BL, Piwnica-Worms D et al (2011) Identification of FUSE-binding protein 1 as a regulatory mRNA-binding protein that represses nucleophosmin translation. Oncogene 30:77–86

    Article  CAS  PubMed  Google Scholar 

  83. Box JK, Paquet N, Adams MN et al (2016) Nucleophosmin: from structure and function to disease development. BMC Mol Biol. https://doi.org/10.1186/s12867-016-0073-9

    Article  PubMed  PubMed Central  Google Scholar 

  84. Williams BY, Hamilton SL, Sarkar HK (2000) The survival motor neuron protein interacts with the transactivator FUSE binding protein from human fetal brain. FEBS Lett 470:207–210. https://doi.org/10.1016/S0014-5793(00)01320-X

    Article  CAS  PubMed  Google Scholar 

  85. Zheng Y, Miskimins WK (2011) Far upstream element binding protein 1 activates translation of p27Kip1 mRNA through its internal ribosomal entry site. Int J Biochem Cell Biol 43:1641–1648. https://doi.org/10.1016/j.biocel.2011.08.001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Huang P-N, Lin J-Y, Locker N et al (2011) Far upstream element binding protein 1 binds the internal ribosomal entry site of enterovirus 71 and enhances viral translation and viral growth. Nucleic Acids Res 39:9633–9648. https://doi.org/10.1093/nar/gkr682

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Tsai F-J, Lin C-W, Lai C-C et al (2011) Kaempferol inhibits enterovirus 71 replication and internal ribosome entry site (IRES) activity through FUBP and HNRP proteins. Food Chem 128:312–322. https://doi.org/10.1016/j.foodchem.2011.03.022

    Article  CAS  PubMed  Google Scholar 

  88. Hung C-T, Kung Y-A, Li M-L et al (2016) Additive promotion of viral internal ribosome entry site-mediated translation by far upstream element-binding protein 1 and an enterovirus 71-induced cleavage product. PLoS Pathog. https://doi.org/10.1371/journal.ppat.1005959

    Article  PubMed  PubMed Central  Google Scholar 

  89. Lin J-Y, Li M-L, Shih S-R (2009) Far upstream element binding protein 2 interacts with enterovirus 71 internal ribosomal entry site and negatively regulates viral translation. Nucleic Acids Res 37:47–59. https://doi.org/10.1093/nar/gkn901

    Article  CAS  PubMed  Google Scholar 

  90. Min H, Turck CW, Nikolic JM, Black DL (1997) A new regulatory protein, KSRP, mediates exon inclusion through an intronic splicing enhancer. Genes Dev 11:1023–1036

    Article  CAS  PubMed  Google Scholar 

  91. Labourier E, Adams MD, Rio DC (2001) Modulation of P-Element Pre-mRNA Splicing by a Direct Interaction between PSI and U1 snRNP 70 K Protein. Mol Cell 8:363–373. https://doi.org/10.1016/S1097-2765(01)00311-2

    Article  CAS  PubMed  Google Scholar 

  92. Rappsilber J, Ryder U, Lamond AI, Mann M (2002) Large-Scale proteomic analysis of the human spliceosome. Genome Res 12:1231–1245. https://doi.org/10.1101/gr.473902

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Pan Q, Shai O, Lee LJ et al (2008) Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nat Genet 40:1413–1415. https://doi.org/10.1038/ng.259

    Article  CAS  PubMed  Google Scholar 

  94. Li H, Wang Z, Zhou X et al (2013) Far upstream element-binding protein 1 and RNA secondary structure both mediate second-step splicing repression. Proc Natl Acad Sci 110:E2687–E2695. https://doi.org/10.1073/pnas.1310607110

    Article  PubMed  PubMed Central  Google Scholar 

  95. Will CL, Lührmann R (2011) Spliceosome structure and function. Cold Spring Harb Perspect Biol. https://doi.org/10.1101/cshperspect.a003707

    Article  PubMed  PubMed Central  Google Scholar 

  96. Wang J, Schultz PG, Johnson KA (2018) Mechanistic studies of a small-molecule modulator of SMN2 splicing. Proc Natl Acad Sci USA 115:E4604–E4612. https://doi.org/10.1073/pnas.1800260115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Freedman DA, Wu L, Levine AJ (1999) Functions of the MDM2 oncoprotein. Cell Mol Life Sci CMLS 55:96–107. https://doi.org/10.1007/s000180050273

    Article  CAS  PubMed  Google Scholar 

  98. Emery AEH (2002) The muscular dystrophies. Lancet Lond Engl 359:687–695. https://doi.org/10.1016/S0140-6736(02)07815-7

    Article  CAS  Google Scholar 

  99. Sutandy FXR, Ebersberger S, Huang L et al (2018) In vitro iCLIP-based modeling uncovers how the splicing factor U2AF2 relies on regulation by cofactors. Genome Res 28:699–713. https://doi.org/10.1101/gr.229757.117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Hwang I, Cao D, Na Y et al (2018) Far upstream element-binding protein 1 regulates LSD1 alternative splicing to promote terminal differentiation of neural progenitors. Stem Cell Rep. https://doi.org/10.1016/j.stemcr.2018.02.013

    Article  PubMed  Google Scholar 

  101. Ostrom QT, Bauchet L, Davis FG et al (2014) The epidemiology of glioma in adults: a “state of the science” review. Neuro-Oncol 16:896–913. https://doi.org/10.1093/neuonc/nou087

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Barbashina V, Salazar P, Holland EC et al (2005) Allelic losses at 1p36 and 19q13 in gliomas: correlation with histologic classification, definition of a 150-kb minimal deleted region on 1p36, and evaluation of CAMTA1 as a candidate tumor suppressor gene. Clin Cancer Res Off J Am Assoc Cancer Res 11:1119–1128

    CAS  Google Scholar 

  103. Sahm F, Koelsche C, Meyer J et al (2012) CIC and FUBP1 mutations in oligodendrogliomas, oligoastrocytomas and astrocytomas. Acta Neuropathol (Berl) 123:853–860. https://doi.org/10.1007/s00401-012-0993-5

    Article  CAS  Google Scholar 

  104. Chan AK-Y, Pang JC-S, Chung NY-F et al (2014) Loss of CIC and FUBP1 expressions are potential markers of shorter time to recurrence in oligodendroglial tumors. Mod Pathol Off J US Can Acad Pathol Inc 27:332–342. https://doi.org/10.1038/modpathol.2013.165

    Article  CAS  Google Scholar 

  105. Brat DJ, Verhaak RGW, Cancer Genome Atlas Research Network et al (2015) Comprehensive, integrative genomic analysis of diffuse lower-grade gliomas. N Engl J Med 372:2481–2498. https://doi.org/10.1056/nejmoa1402121

    Article  CAS  PubMed  Google Scholar 

  106. Suzuki H, Aoki K, Chiba K et al (2015) Mutational landscape and clonal architecture in grade II and III gliomas. Nat Genet 47:458–468. https://doi.org/10.1038/ng.3273

    Article  CAS  PubMed  Google Scholar 

  107. Aihara K, Nagae G (2017) Genetic and epigenetic stability of oligodendrogliomas at recurrence. Acta Neuropathol Commun. https://doi.org/10.1186/s40478-017-0422-z

    Article  PubMed  PubMed Central  Google Scholar 

  108. Bailey MH, Tokheim C, Porta-Pardo E et al (2018) Comprehensive characterization of cancer driver genes and mutations. Cell 173:371–385. https://doi.org/10.1016/j.cell.2018.02.060

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Yip S, Butterfield YS, Morozova O et al (2012) Concurrent CIC mutations, IDH mutations, and 1p/19q loss distinguish oligodendrogliomas from other cancers. J Pathol 226:7–16. https://doi.org/10.1002/path.2995

    Article  CAS  PubMed  Google Scholar 

  110. Chen J, Hackett CS, Zhang S et al (2015) The genetics of splicing in neuroblastoma. Cancer Discov 5:380–395. https://doi.org/10.1158/2159-8290.CD-14-0892

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Bradley RK, Merkin J, Lambert NJ, Burge CB (2012) Alternative splicing of RNA triplets is often regulated and accelerates proteome evolution. PLoS Biol 10:e1001229. https://doi.org/10.1371/journal.pbio.1001229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Bartel F, Taubert H, Harris LC (2002) Alternative and aberrant splicing of MDM2 mRNA in human cancer. Cancer Cell 2:9–15. https://doi.org/10.1016/S1535-6108(02)00091-0

    Article  CAS  PubMed  Google Scholar 

  113. Singh RK, Tapia-Santos A, Bebee TW, Chandler DS (2009) Conserved sequences in the final intron of MDM2 are essential for the regulation of alternative splicing of MDM2 in response to stress. Exp Cell Res 315:3419–3432. https://doi.org/10.1016/j.yexcr.2009.07.017

    Article  CAS  PubMed  Google Scholar 

  114. Steinman HA, Burstein E, Lengner C et al (2004) An alternative splice form of Mdm2 induces p53-independent cell growth and tumorigenesis. J Biol Chem 279:4877–4886. https://doi.org/10.1074/jbc.M305966200

    Article  CAS  PubMed  Google Scholar 

  115. Seiler M, Peng S, Agrawal AA et al (2018) Somatic mutational landscape of splicing factor genes and their functional consequences across 33 cancer types. Cell Rep 23:282–296. https://doi.org/10.1016/j.celrep.2018.01.088

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Liu Z-H, Hu J-L, Liang J-Z et al (2015) Far upstream element-binding protein 1 is a prognostic biomarker and promotes nasopharyngeal carcinoma progression. Cell Death Dis 6:e1920. https://doi.org/10.1038/cddis.2015.258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Pénzváltó Z, Lánczky A, Lénárt J et al (2014) MEK1 is associated with carboplatin resistance and is a prognostic biomarker in epithelial ovarian cancer. BMC Cancer 14:837. https://doi.org/10.1186/1471-2407-14-837

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Zhang J, Xiong X, Hua X et al (2017) Knockdown of FUSE binding protein 1 enhances the sensitivity of epithelial ovarian cancer cells to carboplatin. Oncol Lett 14:5819–5824. https://doi.org/10.3892/ol.2017.6978

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Yu MC, Yuan J-M, Lu SC (2008) Alcohol, cofactors and the genetics of hepatocellular carcinoma. J Gastroenterol Hepatol 23:S92–S97. https://doi.org/10.1111/j.1440-1746.2007.05293.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Sanyal AJ, Yoon SK, Lencioni R (2010) The etiology of hepatocellular carcinoma and consequences for treatment. Oncologist 15:14–22. https://doi.org/10.1634/theoncologist.2010-S4-14

    Article  PubMed  Google Scholar 

  121. Kawate S, Fukusato T, Ohwada S et al (1999) Amplification of c-myc in hepatocellular carcinoma: correlation with clinicopathologic features, proliferative activity and p53 overexpression. Oncology 57:157–163. https://doi.org/10.1159/000012024

    Article  CAS  PubMed  Google Scholar 

  122. El-Serag HB, Rudolph KL (2007) Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology 132:2557–2576. https://doi.org/10.1053/j.gastro.2007.04.061

    Article  CAS  PubMed  Google Scholar 

  123. Murakami H, Sanderson ND, Nagy P et al (1993) Transgenic mouse model for synergistic effects of nuclear oncogenes and growth factors in tumorigenesis: interaction of c-myc and transforming growth factor alpha in hepatic oncogenesis. Cancer Res 53:1719–1723

    CAS  PubMed  Google Scholar 

  124. Zimonjic DB, Keck CL, Thorgeirsson SS, Popescu NC (1999) Novel recurrent genetic imbalances in human hepatocellular carcinoma cell lines identified by comparative genomic hybridization. Hepatol Baltimore, MD 29:1208–1214. https://doi.org/10.1002/hep.510290410

    Article  CAS  Google Scholar 

  125. Schlaeger C, Longerich T, Schiller C et al (2008) Etiology-dependent molecular mechanisms in human hepatocarcinogenesis. Hepatol Baltimore, MD 47:511–520. https://doi.org/10.1002/hep.22033

    Article  CAS  Google Scholar 

  126. Zubaidah RM, Tan GS, Tan SBE et al (2008) 2-D DIGE profiling of hepatocellular carcinoma tissues identified isoforms of far upstream binding protein (FUBP) as novel candidates in liver carcinogenesis. Proteomics 8:5086–5096. https://doi.org/10.1002/pmic.200800322

    Article  CAS  PubMed  Google Scholar 

  127. Wen H, Ma H, Li P et al (2017) Expression of far upstream element-binding protein 1 correlates with c-Myc expression in sacral chordomas and is associated with tumor progression and poor prognosis. Biochem Biophys Res Commun 491:1047–1054. https://doi.org/10.1016/j.bbrc.2017.08.008

    Article  CAS  PubMed  Google Scholar 

  128. Xiong X, Zhang J, Liang W et al (2016) Fuse-binding protein 1 is a target of the EZH2 inhibitor GSK343, in osteosarcoma cells. Int J Oncol 49:623–628

    Article  CAS  PubMed  Google Scholar 

  129. Bièche I, Lachkar S, Becette V et al (1998) Overexpression of the stathmin gene in a subset of human breast cancer. Br J Cancer 78:701–709

    Article  PubMed  PubMed Central  Google Scholar 

  130. Müller B, Bovet M, Yin Y et al (2015) Concomitant expression of far upstream element (FUSE) binding protein (FBP) interacting repressor (FIR) and its splice variants induce migration and invasion of non-small cell lung cancer (NSCLC) cells. J Pathol 237:390–401. https://doi.org/10.1002/path.4588

    Article  CAS  PubMed  Google Scholar 

  131. Brisbin AG, Asmann YW, Song H et al (2011) Meta-analysis of 8q24 for seven cancers reveals a locus between NOV and ENPP2 associated with cancer development. BMC Med Genet 12:156. https://doi.org/10.1186/1471-2350-12-156

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Boelens MC, Kok K, van der Vlies P et al (2009) Genomic aberrations in squamous cell lung carcinoma related to lymph node or distant metastasis. Lung Cancer Amsterdam Netherlands 66:372–378. https://doi.org/10.1016/j.lungcan.2009.02.017

    Article  Google Scholar 

  133. Moinzadeh P, Breuhahn K, Stützer H, Schirmacher P (2005) Chromosome alterations in human hepatocellular carcinomas correlate with aetiology and histological grade—results of an explorative CGH meta-analysis. Br J Cancer 92:935–941. https://doi.org/10.1038/sj.bjc.6602448

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Matsushita K, Tomonaga T, Kajiwara T et al (2009) c-myc suppressor FBP-interacting repressor for cancer diagnosis and therapy. Front Biosci Landmark Ed 14:3401–3408

    Article  CAS  PubMed  Google Scholar 

  135. Saito I, Miyamura T, Ohbayashi A et al (1990) Hepatitis C virus infection is associated with the development of hepatocellular carcinoma. Proc Natl Acad Sci 87:6547–6549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Shi ST, Lai MM (2001) Hepatitis C viral RNA: challenges and promises. Cell Mol Life Sci CMLS 58:1276–1295. https://doi.org/10.1007/PL00000939

    Article  CAS  PubMed  Google Scholar 

  137. Wesely J, Steiner M, Schntgen F et al (2017) Delayed mesoderm and erythroid differentiation of murine embryonic stem cells in the absence of the transcriptional regulator FUBP1. Stem Cells Int 2017:1–12. https://doi.org/10.1155/2017/5762301

    Article  CAS  Google Scholar 

  138. Wilson A, Murphy MJ, Oskarsson T et al (2004) c-Myc controls the balance between hematopoietic stem cell self-renewal and differentiation. Genes Dev 18:2747–2763. https://doi.org/10.1101/gad.313104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Reavie L, Gatta GD, Crusio K et al (2010) Hematopoietic stem cell differentiation regulated by a single ubiquitin ligase: substrate complex. Nat Immunol 11:207–215. https://doi.org/10.1038/ni.1839

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Hoffman B, Amanullah A, Shafarenko M, Liebermann DA (2002) The proto-oncogene c-myc in hematopoietic development and leukemogenesis. Oncogene 21:3414–3421. https://doi.org/10.1038/sj.onc.1205400

    Article  CAS  PubMed  Google Scholar 

  141. Freytag SO (1988) Enforced expression of the c-myc oncogene inhibits cell differentiation by precluding entry into a distinct predifferentiation state in G0/G1. Mol Cell Biol 8:1614–1624

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. Hoffman B, Liebermann DA, Selvakumaran M, Nguyen HQ (1996) Role of c-myc in myeloid differentiation, growth arrest and apoptosis. Curr Top Microbiol Immunol 211:17–27

    CAS  PubMed  Google Scholar 

  143. Eppert K, Takenaka K, Lechman ER et al (2011) Stem cell gene expression programs influence clinical outcome in human leukemia. Nat Med 17:1086–1093. https://doi.org/10.1038/nm.2415

    Article  CAS  PubMed  Google Scholar 

  144. Delgado MD, León J (2010) Myc roles in hematopoiesis and leukemia. Genes Cancer. https://doi.org/10.1177/1947601910377495

    Article  PubMed  PubMed Central  Google Scholar 

  145. Lennartsson J, Jelacic T, Linnekin D, Shivakrupa R (2005) Normal and oncogenic forms of the receptor tyrosine kinase kit. Stem Cells 23:16–43. https://doi.org/10.1634/stemcells.2004-0117

    Article  CAS  PubMed  Google Scholar 

  146. Weidemann RR, Behrendt R, Schoedel KB et al (2017) Constitutive Kit activity triggers B-cell acute lymphoblastic leukemia-like disease in mice. Exp Hematol 45:45–55. https://doi.org/10.1016/j.exphem.2016.09.005

    Article  CAS  PubMed  Google Scholar 

  147. Landau DA, Tausch E, Taylor-Weiner AN et al (2015) Mutations driving CLL and their evolution in progression and relapse. Nature 526:525–530. https://doi.org/10.1038/nature15395

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. Lindqvist CM, Lundmark A, Nordlund J et al (2016) Deep targeted sequencing in pediatric acute lymphoblastic leukemia unveils distinct mutational patterns between genetic subtypes and novel relapse-associated genes. Oncotarget 27:64071–64088. https://doi.org/10.18632/oncotarget.11773

    Article  Google Scholar 

  149. Klener P, Fronkova E, Berkova A et al (2016) Mantle cell lymphoma-variant Richter syndrome: detailed molecular-cytogenetic and backtracking analysis reveals slow evolution of a pre-MCL clone in parallel with CLL over several years: mantle cell lymphoma-variant Richter syndrome. Int J Cancer 139:2252–2260. https://doi.org/10.1002/ijc.30263

    Article  CAS  PubMed  Google Scholar 

  150. Huth JR, Yu L, Collins I et al (2004) NMR-driven discovery of benzoylanthranilic acid inhibitors of far upstream element binding protein binding to the human oncogene c-myc promoter. J Med Chem 47:4851–4857. https://doi.org/10.1021/jm0497803

    Article  CAS  PubMed  Google Scholar 

  151. Au SL-K, Wong CC-L, Lee JM-F et al (2013) EZH2-mediated H3K27me3 is involved in epigenetic repression of deleted in liver cancer 1 in human cancers. PLoS One 8:e68226. https://doi.org/10.1371/journal.pone.0068226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  152. Lv Y-F, Yan G-N, Meng G (2015) Enhancer of zeste homolog two silencing inhibits tumor growth and lung metastasis in osteosarcoma. Sci Rep. https://doi.org/10.1038/srep12999

    Article  PubMed  PubMed Central  Google Scholar 

  153. Niforou KM, Anagnostopoulos AK, Vougas K et al (2008) The proteome profile of the human osteosarcoma U2OS cell line. Cancer Genom Proteom 5:63–78

    CAS  Google Scholar 

  154. Varambally S, Dhanasekaran SM, Zhou M et al (2002) The polycomb group protein EZH2 is involved in progression of prostate cancer. Nature 419:624–629. https://doi.org/10.1038/nature01075

    Article  CAS  PubMed  Google Scholar 

  155. Kleer CG, Cao Q, Varambally S et al (2003) EZH2 is a marker of aggressive breast cancer and promotes neoplastic transformation of breast epithelial cells. Proc Natl Acad Sci USA 100:11606–11611. https://doi.org/10.1073/pnas.1933744100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  156. Khageh Hosseini S, Kolterer S, Steiner M et al (2017) Camptothecin and its analog SN-38, the active metabolite of irinotecan, inhibit binding of the transcriptional regulator and oncoprotein FUBP1 to its DNA target sequence FUSE. Biochem Pharmacol 146:53–62. https://doi.org/10.1016/j.bcp.2017.10.003

    Article  CAS  PubMed  Google Scholar 

  157. Zhou X, Edmonson MN, Wilkinson MR et al (2016) Exploring genomic alteration in pediatric cancer using protein paint. Nat Genet 48:4–6. https://doi.org/10.1038/ng.3466

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. Barretina J, Caponigro G, Stransky N et al (2012) The cancer cell line encyclopedia enables predictive modelling of anticancer drug sensitivity. Nature 483:603–607. https://doi.org/10.1038/nature11003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  159. Idbaih A, Ducray F, Dehais C et al (2012) SNP array analysis reveals novel genomic abnormalities including copy neutral loss of heterozygosity in anaplastic oligodendrogliomas. PLoS One 7:e45950. https://doi.org/10.1371/journal.pone.0045950

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  160. Cahill DP, Louis DN, Cairncross JG (2015) Molecular background of oligodendroglioma: 1p/19q, IDH, TERT, CIC and FUBP1. CNS Oncol 4:287–294. https://doi.org/10.2217/cns.15.32

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  161. Erdem-Eraslan L, Heijsman D, de Wit M et al (2015) Tumor-specific mutations in low-frequency genes affect their functional properties. J Neurooncol 122:461–470. https://doi.org/10.1007/s11060-015-1741-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  162. Zhang L, Liu Y, Wang M (2017) EZH2-, CHD4-, and IDH-linked epigenetic perturbation and its association with survival in glioma patients. J Mol Cell Biol. https://doi.org/10.1093/jmcb/mjx056

    Article  PubMed  PubMed Central  Google Scholar 

  163. Ma J, Chen M, Xia S-K et al (2013) Prostaglandin E2 promotes liver cancer cell growth by the upregulation of FUSE-binding protein 1 expression. Int J Oncol 42:1093–1104

    Article  CAS  PubMed  Google Scholar 

  164. Samarin J, Laketa V, Malz M et al (2016) PI3K/AKT/mTOR-dependent stabilization of oncogenic far-upstream element binding proteins in hepatocellular carcinoma cells. Hepatology 63:813–826. https://doi.org/10.1002/hep.28357

    Article  CAS  PubMed  Google Scholar 

  165. Zhang F, Tian Q, Wang Y (2013) Far upstream element-binding protein 1 (FUBP1) is overexpressed in human gastric cancer tissue compared to non-cancerous tissue. Onkologie 36:650–655. https://doi.org/10.1159/000355659

    Article  CAS  PubMed  Google Scholar 

  166. Jia MY, Wang YJ (2014) Far upstream element-binding protein 1(FUBP1) expression differs between human colorectal cancer and non-cancerous tissue. Neoplasma 61:533–540. https://doi.org/10.4149/neo_2014_065

    Article  CAS  PubMed  Google Scholar 

  167. Gagné J-P, Gagné P, Hunter JM et al (2005) Proteome profiling of human epithelial ovarian cancer cell line TOV-112D. Mol Cell Biochem 275:25–55

    Article  PubMed  Google Scholar 

  168. Zhong Q, Liu Z, Lin Z-R et al (2017) The RARS-MADlLl fusion gene induces cancer stem cell-like properties and therapeutic resistance in nasopharyngeal carcinoma. Clin Cancer Res. https://doi.org/10.1158/1078-0432.ccr-17-0352

    Article  PubMed  PubMed Central  Google Scholar 

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Funding

This work was supported by Ligue Régionale contre le cancer (comité 22, 35, 56, 79, 41) (MBT, LD), SFR Biosit UMS CNRS 3480—INSERM 018 (MBT), Région Bretagne (LD, MBT), The Société Française d’Hématologie (LD), Rennes Métropole (MBT), the société française de lutte contre les cancers et les leucémies de l’enfant et de l’adolescent and the Fédération Enfants et Santé (MBT), a private donator Mrs. M-Dominique Blanc-Bert (MBT), Cancéropole Grand Ouest (LD), and the CNRS, Université de Rennes 1 and the People Programme (Marie Curie Actions) of the European Union’s Seventh Framework Programme (FP7/2007-2013) under REA grant agreement no. 291851 (MBT).

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  1. Univ Rennes, CNRS, IGDR (Institut de Génétique et Développement de Rennes)-UMR 6290, F-35000, Rennes, France

    Lydie Debaize & Marie-Bérengère Troadec

  2. Univ Brest, INSERM, EFS, UMR 1078, GGB, F-29200, Brest, France

    Marie-Bérengère Troadec

  3. CHRU de Brest, laboratoire de cytogénétique, F-29200, Brest, France

    Marie-Bérengère Troadec

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  1. Lydie Debaize
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Debaize, L., Troadec, MB. The master regulator FUBP1: its emerging role in normal cell function and malignant development. Cell. Mol. Life Sci. 76, 259–281 (2019). https://doi.org/10.1007/s00018-018-2933-6

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