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Tumor Biology

, Volume 37, Issue 6, pp 8375–8382 | Cite as

ABCE1 plays an essential role in lung cancer progression and metastasis

  • Ye Tian
  • Xin Tian
  • Xu Han
  • Yong Chen
  • Cheng-Yang Song
  • Wen-Jun Jiang
  • Da-Li Tian
Original Article

Abstract

ATP-binding cassette E1 (ABCE1) is a member of the ATP-binding cassette transporters and regulates a broad range of biological functions including viral infection, cell proliferation, and anti-apoptosis. We have previously shown that ABCE1 is a prognostic indicator for lung cancer, although the underlying mechanisms remain unclear. To investigate whether the ABCE1 gene contributes to the malignancy of lung tumors, we introduced ABCE1 into LTEP-a-2 lung adenocarcinoma cells. Ectopic ABCE1 expression promoted clonogenicity and anchorage-independent growth of LTEP-a-2 cells, while in a mouse xenograft tumor model, it had an augmentative effect on tumor growth and metastasis and reduced the expression of the tumor-suppressor gene growth arrest and DNA damage-inducible 45α (GADD45α). Moreover, apoptosis was not significantly influenced by ABCE1 in vitro. In summary, we have provided evidence that ABCE1 plays an essential role in the progression and metastasis of lung cancers and may represent a valuable therapeutic target for the management of lung tumor.

Keywords

ABCE1 Lung cancer Progression Metastasis 

Notes

Acknowledgments

This study was supported by the Young Innovation and Development Foundation from the Fourth Affiliated Hospital of China Medical University and the National Nature Science Foundation of China (#30973502).

Compliance with ethical standards

BALB/C nude mice were obtained from the animal facility of China Medical University and were treated according to the ethical guidelines of the institution.

Conflicts of interest

None

References

  1. 1.
    Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, et al. Global cancer statistics, 2012. CA Cancer J Clin. 2015;65(2):87–108.CrossRefPubMedGoogle Scholar
  2. 2.
    Filipits M, Pirker R, Dunant A, Lantuejoul S, Schmid K, et al. Cell cycle regulators and outcome of adjuvant cisplatin-based chemotherapy in completely resected non-small-cell lung cancer: the International Adjuvant Lung Cancer Trial Biologic Program. J Clin Oncol. 2007;25(19):2735–40.CrossRefPubMedGoogle Scholar
  3. 3.
    Li MJ, Tian DL, Fu WN. Screening of metastasis-related genes in small cell lung cancer by differential display. J Chin Med Univ. 2006;35(1):31–5.Google Scholar
  4. 4.
    Bisbal C, Martinand C, Silhol M, Lebleu B, Salehzada T. Cloning and characterization of a RNAse L inhibitor. A new component of the interferon-regulated 2–5A pathway. J Biol Chem. 1995;270(22):13308–17.CrossRefPubMedGoogle Scholar
  5. 5.
    Hassel BA, Zhou A, Sotomayor C, Maran A, Silverman RH. A dominant negative mutant of 2-5A-dependent RNase suppresses antiproliferative and antiviral effects of interferon. EMBO J. 1995;12(8):3297–304.Google Scholar
  6. 6.
    Le Roy F, Bisbal C, Silhol M, Martinand C, Lebleu B, Salehzada T. The 2-5A/RNase L/RNase L inhibitor (RLI) [correction of (RNI)] pathway regulates mitochondrial mRNAs stability in interferon alpha-treated H9 cells. J Biol Chem. 2001;276(51):48473–82.PubMedGoogle Scholar
  7. 7.
    Huang B, Gao Y, Tian DL, Zheng M. A small interfering ABCE1-targeting RNA inhibits the proliferation and invasiveness of small cell lung cancer. Int J Mol Med. 2010;25(5):687–93.PubMedGoogle Scholar
  8. 8.
    Ren Y, Li YH, Tian DL. Role of the ABCE1 gene in human lung adenocarcinoma. Oncol Rep. 2012;27(4):965–70.PubMedPubMedCentralGoogle Scholar
  9. 9.
    Hlavata I, Mohelnikova-Duchonova B, Vaclavikova R, Liska V, Pitule P, et al. The role of ABC transporters in progression and clinical outcome of colorectal cancer. Mutagenesis. 2012;27(2):187–96.CrossRefPubMedGoogle Scholar
  10. 10.
    Furuta M, Kozaki KI, Tanaka S, Arii S, Imoto I, et al. miR-124 and miR-203 are epigenetically silenced tumor-suppressive microRNAs in hepatocellular carcinoma. Carcinogenesis. 2010;31(5):766–76.CrossRefPubMedGoogle Scholar
  11. 11.
    Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, et al. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell. 2004;117(7):927–39.CrossRefPubMedGoogle Scholar
  12. 12.
    Huang B, Zhou HL, Lang XP, Liu ZL. siRNA-induced ABCE1 silencing inhibits proliferation and invasion of breast cancer cells. Mol Med Rep. 2014;10(4):1685–90.PubMedPubMedCentralGoogle Scholar
  13. 13.
    Wang L, Zhang M, Liu DX. Knock-down of ABCE1 gene induces G1/S arrest in human oral cancer cells. Int J Clin Exp Pathol. 2014;7(9):5495–504.PubMedPubMedCentralGoogle Scholar
  14. 14.
    Tian Y, Han X, Tian DL. The biological regulation of ABCE1. IUBMB life. 2012;64(10):795–800.CrossRefPubMedGoogle Scholar
  15. 15.
    Becker T, Franckenberg S, Wickles S, Shoemaker CJ, Anger AM, et al. Structure basis of highly conserved ribosome recycling in eukaryotes and archaea. Nature. 2012;482(7386):501–6.CrossRefPubMedGoogle Scholar
  16. 16.
    Karcher A, Schele A, Hopfner KP. X-ray structure of the complete ABC enzyme ABCE1 from Pyrococcus abyssi. J Biol Chem. 1996;283(12):7962–71.CrossRefGoogle Scholar
  17. 17.
    Nürenberg E, Tampé R. Tying up loose ends: ribosome recycling in eukaryotes and archaea. Trends Biochem Sci. 2013;38(2):64–74.CrossRefPubMedGoogle Scholar
  18. 18.
    Franckenberg S, Becker T, Beckmann R. Structural view on recycling of archaeal and eukaryotic ribosomes after canonical termination and ribosome rescue. Curr Opin Struct Biol. 2012;22(6):786–96.CrossRefPubMedGoogle Scholar
  19. 19.
    Chen Z, Dong J, Ishimura A, Daar I, Hinnebusch AG, et al. The essential vertebrate ABCE1 protein interacts with eukaryotic initiation factors. J Biol Chem. 2006;281(11):7452–7.CrossRefPubMedGoogle Scholar
  20. 20.
    Tian Y, Tian X, Han X, Chen Y, Song CY, et al. Expression of ATP binding cassette E1 (ABCE1) enhances viability and invasion of lung adenocarcinoma cells in vitro. Mol Med Rep. 2015; in press.Google Scholar
  21. 21.
    Tamura RE, de Vasconcellos JF, Sarkar D, Libermann TA, fisher PB, et al. GADD45 proteins: central players in tumorigenesis. Curr Mol Med. 2012; 12(5): 634–651.Google Scholar
  22. 22.
    Higashi H, Vallbohmer D, Warnecke-Eberz U, Hokita S, Xi H, et al. Down-regulation of Gadd45 expression is associated with tumor differentiation in non-small cell lung cancer. Anticancer Res. 2006;26(3A):2143–7.PubMedGoogle Scholar
  23. 23.
    Smith ML, Ford JM, Hollander MC, Bortnick RA, Amundson SA, et al. p53-mediated DNA repair responses to UV radiation: studies of mouse cells lacking p53, p21, and/orgadd45 Genes. Mol Cell Biol. 2000;20(10):3705–14.CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Rai K, Huggins IJ, James SR, Karpf AR, Jones DA, et al. DNA demethylation in zebrafish involves the coupling of a deaminase, a glycosylase, and gadd45. Cell. 2008;135(7):1201–12.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Wang XW, Zhan Q, Coursen JD, Khan MA, Kontny HU, et al. GADD45 induction of a G2/M cell cycle checkpoint. Proc Natl Acad Sci U S A. 1999;96(7):3706–11.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Jin S, Tong T, Fan W, Fan F, Antinore MJ, et al. GADD45-induced cell cycle G2-M arrest associates with altered subcellular distribution of cyclin B1 and is independent of p38 kinase activity. Oncogene. 2002;21(57):8696–704.CrossRefPubMedGoogle Scholar
  27. 27.
    Sakaue M, Adachi H, Jetten AM. Post-transcriptional regulation of MyD118 and GADD45 in human lung carcinoma cells during 6-[3-(1-adamantyl)-4-hydroxyphenyl]-2-naphthalene carboxylic acid-induced apoptosis. Mol Pharmacol. 1999;55(4):668–76.PubMedGoogle Scholar
  28. 28.
    Oki T, Sowa Y, Hirose T, Takaqaki N, Horinaka M, et al. Genistein induces gadd45 gene and G2/M cell cycle arrest in the DU145 human prostate cancer cell line. FEBS Lett. 2004;577(1–2):55–9.CrossRefPubMedGoogle Scholar
  29. 29.
    Ramachandran K, Gopisetty G, Gordian E, Navarro L, Hader C, et al. Methylation-mediated repression of GADD45alpha in prostate cancer and its role as a potential therapeutic target. Cancer Res. 2009;69(4):1527–35.CrossRefPubMedGoogle Scholar

Copyright information

© International Society of Oncology and BioMarkers (ISOBM) 2016

Authors and Affiliations

  • Ye Tian
    • 1
  • Xin Tian
    • 2
  • Xu Han
    • 1
  • Yong Chen
    • 1
  • Cheng-Yang Song
    • 1
  • Wen-Jun Jiang
    • 1
  • Da-Li Tian
    • 1
  1. 1.Department of Thoracic SurgeryThe Fourth Affiliated Hospital of China Medical UniversityShenyangChina
  2. 2.Molecular Oncology Department of Cancer Research Institutethe First Affiliated Hospital of China Medical UniversityShenyangChina

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