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Tumor Biology

, Volume 36, Issue 8, pp 6223–6230 | Cite as

Antagomir-1290 suppresses CD133+ cells in non-small cell lung cancer by targeting fyn-related Src family tyrosine kinase

  • Bo Sun
  • Nan Yang
  • Yao Jiang
  • Huifeng Zhang
  • Chunying Hou
  • Chao Ji
  • Yanyong Liu
  • Pingping Zuo
Research Article

Abstract

Cancer stem-like cells (CSLCs) are involved in cancer initiation, development, and metastasis, and microRNAs (miRNAs) play pivotal roles in regulating CSLCs. miRNA-based therapeutic strategy associated with CSLCs might promise potential new therapeutic approaches. In the present study, we found that miR-1290 was increased in CD133+ cells. Antagomir-1290 significantly suppressed tumor volume and weight initiated by CD133+ cells in vivo. Furthermore, antagomir-1290 significantly inhibited the proliferation, clonogenicity, invasion, and migration of CD133+ cells by targeting fyn-related Src family tyrosine kinase. These findings provide insights into the clinical prospect of miR-1290-based therapies for non-small cell lung cancer.

Keywords

Cancer stem-like cells miR-1290 Fyn-related Src family tyrosine kinase Non-small cell lung cancer 

Notes

Acknowledgments

This study was supported by the National Basic Research Program of China (973 Program, 2010CB934002).

Conflicts of interest

None

References

  1. 1.
    Siegel R, Ma J, Zou Z, Jemal A. Cancer statistics, 2014. CA Cancer J Clin. 2014;64(1):9–29.CrossRefPubMedGoogle Scholar
  2. 2.
    Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature. 2001;414(6859):105–11.CrossRefPubMedGoogle Scholar
  3. 3.
    Yin AH, Miraglia S, Zanjani ED, Almeida-Porada G, Oqawa M, Leary AG, et al. AC133, a novel marker for human hematopoietic stem and progenitor cells. Blood. 1997;90(12):5002–12.PubMedGoogle Scholar
  4. 4.
    Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, et al. Identification of human brain tumour initiating cells. Nature. 2004;432(7015):396–401.CrossRefPubMedGoogle Scholar
  5. 5.
    Collins AT, Berry PA, Hyde C, Stower MJ, Maitland NJ. Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res. 2005;65(23):10946–51.CrossRefPubMedGoogle Scholar
  6. 6.
    Yin S, Li J, Hu C, Chen X, Yao M, Yan M, et al. CD133 positive hepatocellular carcinoma cells possess high capacity for tumorigenicity. Int J Cancer. 2007;120(7):1444–50.CrossRefPubMedGoogle Scholar
  7. 7.
    Hermann PC, Huber SL, Herrier T, Aicher A, Ellwart JW, Guba M, et al. Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell. 2007;1(3):313–23.CrossRefPubMedGoogle Scholar
  8. 8.
    Ricci-Vitiani L, Lombardi DG, Pilozzi E, Biffoni M, Todaro M, Peschle C, et al. Identification and expansion of human colon-cancer-initiating cells. Nature. 2007;445(7123):111–5.CrossRefPubMedGoogle Scholar
  9. 9.
    Tirino V, Camerlingo R, Franco R, Malanga D, LaRocca A, Viglietto G, et al. The role of CD133 in the identification and characterization of tumour-initiating cells in non-small-cell lung cancer. Eur J Cardiothorac Surg. 2009;36(3):446–53.CrossRefPubMedGoogle Scholar
  10. 10.
    Zhang H, Yang N, Sun B, Jiang Y, Hou C, Ji C, et al. CD133 positive cells isolated from A549 cell line exhibited high liver metastatic potential. Neoplasma. 2014;61(2):153–60.CrossRefPubMedGoogle Scholar
  11. 11.
    Valencia-Sanchez MA, Liu J, Hannon GJ, Parker R. Control of translation and mRNA degradation by miRNAs and siRNAs. Genes Dev. 2006;20(5):515–24.CrossRefPubMedGoogle Scholar
  12. 12.
    Kent OA, Mendell JT. A small piece in the cancer puzzle: microRNAs as tumor suppressors and oncogenes. Oncogene. 2006;25(46):6188–96.CrossRefPubMedGoogle Scholar
  13. 13.
    Yu F, Yao H, Zhu P, Zhang X, Pan Q, Gong C, et al. Let-7 regulates self renewal and tumorgenicity of breast cancer cells. Cell. 2007;131(6):1109–23.CrossRefPubMedGoogle Scholar
  14. 14.
    Liu C, Kelnar K, Liu B, Chen X, Calhoun-Davis T, Li H, et al. The microRNA miR-34a inhibits prostate cancer stem cells and metastasis by directly repressing CD44. Nat Med. 2011;17(2):211–5.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Jackson AL, Bartz SR, Schelter J, Kobayashi SV, Burchard J, Mao M, et al. Expression profiling reveals off-target gene regulation by RNAi. Nat Biotechnol. 2003;21(6):635–7.CrossRefPubMedGoogle Scholar
  16. 16.
    Li A, Yu J, Kim H, Wolfgang CL, Canto MI, Hruban RH, et al. MicroRNA array analysis finds elevated serum miR-1290 accurately distinguishes patients with low-stage pancreatic cancer from healthy and disease controls. Clin Cancer Res. 2013;19(13):3600–10.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Wu J, Ji X, Zhu L, Jiang Q, Wen Z, Xu S, et al. Up-regulation of microRNA-1290 impairs cytokinesis and affects the reprogramming of colon cancer cells. Cancer Lett. 2013;329(2):155–63.CrossRefPubMedGoogle Scholar
  18. 18.
    An IS, An S, Kwon KJ, Kim YJ, Bae S. Ginsenoside Rh2 mediates changes in the microRNA expression profile of human non-small cell lung cancer A549 cells. Oncol Rep. 2013;29(2):523–8.PubMedGoogle Scholar
  19. 19.
    Kim KB, Kim K, Bae S, Choi Y, Cha HJ, Kim SY, et al. MicroRNA-1290 promotes asiatic acid-induced apoptosis by decreasing BCL2 protein level in A549 non-small cell lung carcinoma cells. Oncol Rep. 2014;32(3):1029–36.PubMedGoogle Scholar
  20. 20.
    Martin Del Campo SE, Latchana N, Levine KM, Grignol VP, Fairchild ET, Jaime-Ramirez AC, et al. MiR-21 enhances melanoma invasiveness via inhibition of tissue inhibitor of metalloproteinases 3 expression: in vivo effects of miR-21 inhibitor. PLoS One. 2015;10(1):e0115919.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Ju SY, Chiou SH, Su Y. Maintenance of the stemness in CD44+ HCT-15 and HCT-116 human colon cancer cells requires miR-203 suppression. Stem Cell Res. 2013;12(1):86–100.CrossRefPubMedGoogle Scholar
  22. 22.
    Cance WG, Craven RJ, Weiner TM, Liu ET. Novel protein kinases expressed in human breast cancer. Int J Cancer. 1993;54(4):571–7.CrossRefPubMedGoogle Scholar
  23. 23.
    Meyer T, Xu L, Chang J, Liu ET, Craven RJ, Cance WG. Breast cancer cell line proliferation blocked by the Src-related Rak tyrosine kinase. Int J Cancer. 2003;104(2):139–46.CrossRefPubMedGoogle Scholar
  24. 24.
    Zhou X, Hua L, Zhang W, Zhu M, Shi Q, Li F, et al. FRK controls migration and invasion of human glioma cells by regulating JNK/c-Jun signaling. J Neurooncol. 2012;110(1):9–19.CrossRefPubMedGoogle Scholar
  25. 25.
    Anneren C, Lindholm CK, Kriz V, Welsh M. The FRK/RAK-SHB signaling cascade: a versatile signal-transduction pathway that regulates cell survival, differentiation and proliferation. Curr Mol Med. 2003;3(4):313–24.CrossRefPubMedGoogle Scholar
  26. 26.
    Yim EK, Siwko S, Lin SY. Exploring Rak tyrosine kinase function in breast cancer. Cell Cycle. 2009;8(15):2360–4.CrossRefPubMedGoogle Scholar
  27. 27.
    Garg M. Targeting microRNAs in epithelial-to-mesenchymal transition-induced cancer stem cells: therapeutic approaches in cancer. Expert Opion Ther Targets. 2015;19(2):285–97.CrossRefGoogle Scholar
  28. 28.
    Hunag X, Yuan T, Liang M, Du M, Xia S, Dittmar R, et al. Exosomal miR-1290 and miR-375 as prognostic markers in castration-resistant prostate cancer. Eur Urol. 2014;67(1):33–41.CrossRefGoogle Scholar
  29. 29.
    Endo Y, Yamashita H, Takahashi S, Sato S, Yoshimoto N, Asano T, et al. Immunohistochemical determination of the miR-1290 target arylamine N-acetyltransferase 1 (NAT1) as a prognpstic biomarker in breast cancer. BMC Cancer. 2014;14:990.CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Yim EK, Peng G, Dai H, Hu R, Li K, Mills GB, et al. Rak functions as a tumor suppressor by regulating PTEN protein stability and function. Cancer Cell. 2009;15(4):304–14.CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Xu J, Li Z, Wang J, Chen H, Fang JY. Combined PTEN mutation and protein expression associate with overall and disease-free survival of glioblastoma patients. Transl Oncol. 2014;7(2):196–205.CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Pardella LM, Evangelisti C, Logorio C, Ceccarelli C, Neri I, Zuntini R, et al. A novel deleterious PTEN mutation in a patient with early-onset bilateral breast cancer. BMC Cancer. 2014;14:70.CrossRefGoogle Scholar
  33. 33.
    Yun F, Jia Y, Li X, Yuan L, Sun Q, Yu H, et al. Clinicopathological significance of PTEN and PI3K/AKT signal transduction pathway in non-small cell lung cancer. Int J Clin Exp Pathol. 2013;6(10):2112–20.PubMedPubMedCentralGoogle Scholar
  34. 34.
    Liu Y, Wang X, Yang D, Xiao Z, Chen X. microRNA-21 affects proliferation and apotosis by regulating expression of PTEN in human keloid fibroblasts. Plast Reconstr Surg. 2014;134(4):561e–73.CrossRefPubMedGoogle Scholar
  35. 35.
    Knuefermann C, Liu Y, Liu B, Jin W, Liang K, Wu L, et al. HER2/PI-3K/AKT activation leads to a multidrug resistance in human breast adenocarcinoma cells. Oncogene. 2003;22(21):3205–15.CrossRefPubMedGoogle Scholar
  36. 36.
    Hu L, Hofmann J, Lu Y, Mills GB, Jaffe RB. Inhibition of phosphatidylinositol 3’-kinase increase efficacy of paclitaxel in vitro and in vivo ovarian cancer models. Cancer Res. 2002;62(4):1087–92.PubMedGoogle Scholar
  37. 37.
    Ng SSW, Tsao MS, Chow S, Hedley DW. Inhibition of phosphatidylinositide 3-kinase enhances gemcitabine-induced apoptosis in human pancreatic cancer cells. Cancer Res. 2000;60(19):5451–5.PubMedGoogle Scholar
  38. 38.
    Bozulic L, Hemmings BA. PIKKing on PKB: regulation of PKB activity by phosphorylation. Curr Opin Cell Biol. 2009;21(2):256–61.CrossRefPubMedGoogle Scholar

Copyright information

© International Society of Oncology and BioMarkers (ISOBM) 2015

Authors and Affiliations

  1. 1.Department of Pharmacology, Institute of Basic Medical SciencesChinese Academy of Medical Sciences and Peking Union Medical CollegeBeijingPeople’s Republic of China

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