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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

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Tumor Biology

Abstract

The human far upstream element (FUSE) binding protein 1 (FUBP1) belongs to an ancient family which is required for proper regulation of the c-Myc proto-oncogene. Although c-Myc plays an important role in development of various carcinomas, the relevance of FUBP1 and their contribution to esophageal squamous cell carcinoma (ESCC) development remain unclear. In this study, we aimed to investigate the relationship between FUBP1 and c-Myc as well as their contribution to ESCC development. Western blot and immunohistochemical analyses were performed to evaluate FUBP1 expression. Coimmunoprecipitation analysis was performed to explore the correlation between FUBP1 and c-Myc in ESCC. In addition, the role of FUBP1 in ESCC proliferation was studied in ESCC cells through knocking FUBP1 down. The regulation of FUBP1 on proliferation was confirmed by Cell Counting Kit-8 (CCK-8) assay, flow cytometric assays, and clone formation assays. The expressions of FUBP1 and c-Myc were both upregulated in ESCC tissues. In addition to correlation between expression of FUBP1 and tumor grade, we also confirmed the correlation of FUBP1, c-Myc, and Ki-67 expression by twos. Moreover, upregulation of FUBP1 and c-Myc in ESCC was associated with poor survival. FUBP1 was confirmed to activate c-Myc in ESCC tissues and cells. FUBP1 was demonstrated to promote proliferation of ESCC cells. Moreover, downregulation of both FUBP1 and c-Myc was confirmed to inhibit proliferation of ESCC cells. Our results indicated that FUBP1 may potentially stimulate c-Myc expression in ESCC and its expression may promote ESCC progression.

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References

  1. Jemal A, Siegel R, Ward E, Murray T, Xu J, Thun MJ. Cancer statistics, 2007. CA Cancer J Clin. 2007;57(1):43–66.

    Article  PubMed  Google Scholar 

  2. Zhang L, Wu YD, Li P, Tu J, Niu YL, Xu CM, et al. Effects of cyclooxygenase-2 on human esophageal squamous cell carcinoma. World J Gastroenterol WJG. 2011;17(41):4572–80. doi:10.3748/wjg.v17.i41.4572.

    Article  CAS  PubMed  Google Scholar 

  3. Avigan MI, Strober B, Levens D. A far upstream element stimulates c-myc expression in undifferentiated leukemia cells. J Biol Chem. 1990;265(30):18538–45.

    CAS  PubMed  Google Scholar 

  4. Duncan R, Bazar L, Michelotti G, Tomonaga T, Krutzsch H, Avigan M, et al. A sequence-specific, single-strand binding protein activates the far upstream element of c-myc and defines a new DNA-binding motif. Genes Dev. 1994;8(4):465–80.

    Article  CAS  PubMed  Google Scholar 

  5. Chien HL, Liao CL, Lin YL. FUSE binding protein 1 interacts with untranslated regions of Japanese encephalitis virus RNA and negatively regulates viral replication. J Virol. 2011;85(10):4698–706. doi:10.1128/JVI.01950-10.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Cao G, Kuriyama S, Du P, Sakamoto T, Kong X, Masui K, et al. Complete regression of established murine hepatocellular carcinoma by in vivo tumor necrosis factor alpha gene transfer. Gastroenterology. 1997;112(2):501–10.

    Article  CAS  PubMed  Google Scholar 

  7. Yamanaka T, Shiraki K, Sugimoto K, Ito T, Fujikawa K, Ito M, et al. Chemotherapeutic agents augment TRAIL-induced apoptosis in human hepatocellular carcinoma cell lines. Hepatology. 2000;32(3):482–90. doi:10.1053/jhep.2000.16266.

    Article  CAS  PubMed  Google Scholar 

  8. Sheikh MS, Huang Y. Death receptors as targets of cancer therapeutics. Curr Cancer Drug Targets. 2004;4(1):97–104.

    Article  CAS  PubMed  Google Scholar 

  9. Ohira M, Ohdan H, Mitsuta H, Ishiyama K, Tanaka Y, Igarashi Y, et al. Adoptive transfer of TRAIL-expressing natural killer cells prevents recurrence of hepatocellular carcinoma after partial hepatectomy. Transplantation. 2006;82(12):1712–9. doi:10.1097/01.tp.0000250935.41034.2d.

    Article  CAS  PubMed  Google Scholar 

  10. Sturm I, Stephan C, Gillissen B, Siebert R, Janz M, Radetzki S, et al. Loss of the tissue-specific proapoptotic BH3-only protein Nbk/Bik is a unifying feature of renal cell carcinoma. Cell Death Differ. 2006;13(4):619–27. doi:10.1038/sj.cdd.4401782.

    Article  CAS  PubMed  Google Scholar 

  11. Rabenhorst U, Beinoraviciute-Kellner R, Brezniceanu ML, Joos S, Devens F, Lichter P, et al. Overexpression of the far upstream element binding protein 1 in hepatocellular carcinoma is required for tumor growth. Hepatology. 2009;50(4):1121–9. doi:10.1002/hep.23098.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Malz M, Weber A, Singer S, Riehmer V, Bissinger M, Riener MO, et al. Overexpression of far upstream element binding proteins: a mechanism regulating proliferation and migration in liver cancer cells. Hepatology. 2009;50(4):1130–9. doi:10.1002/hep.23051.

    Article  CAS  PubMed  Google Scholar 

  13. Singer S, Malz M, Herpel E, Warth A, Bissinger M, Keith M, et al. Coordinated expression of stathmin family members by far upstream sequence element-binding protein-1 increases motility in non-small cell lung cancer. Cancer Res. 2009;69(6):2234–43. doi:10.1158/0008-5472.CAN-08-3338.

    Article  CAS  PubMed  Google Scholar 

  14. Belletti B, Nicoloso MS, Schiappacassi M, Berton S, Lovat F, Wolf K, et al. Stathmin activity influences sarcoma cell shape, motility, and metastatic potential. Mol Biol Cell. 2008;19(5):2003–13. doi:10.1091/mbc.E07-09-0894.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Zhang J, Chen QM. Far upstream element binding protein 1: a commander of transcription, translation and beyond. Oncogene. 2013;32(24):2907–16. doi:10.1038/onc.2012.350.

    Article  CAS  PubMed  Google Scholar 

  16. Nie Z, Hu G, Wei G, Cui K, Yamane A, Resch W, et al. c-Myc is a universal amplifier of expressed genes in lymphocytes and embryonic stem cells. Cell. 2012;151(1):68–79. doi:10.1016/j.cell.2012.08.033.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Ding Z, Liu X, Liu Y, Zhang J, Huang X, Yang X, et al. Expression of far upstream element (FUSE) binding protein 1 in human glioma is correlated with c-Myc and cell proliferation. Mol Carcinog. 2013. doi:10.1002/mc.22114.

    Google Scholar 

  18. Wang Y, Yang S, Ni Q, He S, Zhao Y, Yuan Q, et al. Overexpression of forkhead box J2 can decrease the migration of breast cancer cells. J Cell Biochem. 2012;113(8):2729–37. doi:10.1002/jcb.24146.

    Article  CAS  PubMed  Google Scholar 

  19. Zhu H, Wang Q, Hu C, Zhang W, Quan L, Liu M, et al. High expression of survivin predicts poor prognosis in esophageal squamous cell carcinoma following radiotherapy. Tumour Biol J Intern Soc Oncodevelop Biol Med. 2011;32(6):1147–53. doi:10.1007/s13277-011-0217-y.

    Article  CAS  Google Scholar 

  20. Dong C, Yuan T, Wu Y, Wang Y, Fan TW, Miriyala S, et al. Loss of FBP1 by snail-mediated repression provides metabolic advantages in basal-like breast cancer. Cancer Cell. 2013;23(3):316–31. doi:10.1016/j.ccr.2013.01.022.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Engidawork E, Afjehi-Sadat L, Yang JW, Slavc I, Lubec G. Protein chemical identification and characterization of the human variants of far upstream element binding protein in medulloblastoma DAOY cell line. Int J Oncol. 2006;29(3):721–36.

    CAS  PubMed  Google Scholar 

  22. Niforou KM, Anagnostopoulos AK, Vougas K, Kittas C, Gorgoulis VG, Tsangaris GT. The proteome profile of the human osteosarcoma U2OS cell line. Cancer Genomics Proteomics. 2008;5(1):63–78.

    CAS  PubMed  Google Scholar 

  23. Zheng Y, Miskimins WK. Far upstream element binding protein 1 activates translation of p27Kip1 mRNA through its internal ribosomal entry site. Int J Biochem Cell Biol. 2011;43(11):1641–8. doi:10.1016/j.biocel.2011.08.001.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Weber A, Kristiansen I, Johannsen M, Oelrich B, Scholmann K, Gunia S, et al. The FUSE binding proteins FBP1 and FBP3 are potential c-myc regulators in renal, but not in prostate and bladder cancer. BMC Cancer. 2008;8:369. doi:10.1186/1471-2407-8-369.

    Article  PubMed  PubMed Central  Google Scholar 

  25. He L, Liu J, Collins I, Sanford S, O’Connell B, Benham CJ, et al. Loss of FBP function arrests cellular proliferation and extinguishes c-myc expression. EMBO J. 2000;19(5):1034–44. doi:10.1093/emboj/19.5.1034.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This study was supported by the National Natural Science Foundation of China (No. 81272708).

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Correspondence to Run-zhou Ni or Li-li Ji.

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Lei Yang and Jun-ya Zhu contributed equally to this work.

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Yang, L., Zhu, Jy., Zhang, Jg. et al. 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 (2016). https://doi.org/10.1007/s13277-015-4263-8

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  • DOI: https://doi.org/10.1007/s13277-015-4263-8

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