DOI QR코드

DOI QR Code

MiR-150-5p Suppresses Colorectal Cancer Cell Migration and Invasion through Targeting MUC4

  • Wang, Wei-Hua (Department of Clinical Laboratory, The Affiliated Hospital of Ningbo University) ;
  • Chen, Jie (Department of Clinical Laboratory, The Affiliated Hospital of Ningbo University) ;
  • Zhao, Feng (Department of Clinical Laboratory, The Affiliated Hospital of Ningbo University) ;
  • Zhang, Bu-Rong (Department of Clinical Laboratory, The Affiliated Hospital of Ningbo University) ;
  • Yu, Hong-Sheng (Department of Clinical Laboratory, The Affiliated Hospital of Ningbo University) ;
  • Jin, Hai-Ying (Department of Clinical Laboratory, The Affiliated Hospital of Ningbo University) ;
  • Dai, Jin-Hua (Department of Clinical Laboratory, Ningbo No.2 Hospital)
  • Published : 2014.08.15

Abstract

Growing evidence suggests that miR-150-5p has an important role in regulating genesis of various types of cancer. However, the roles and the underlying mechanisms of miR-150-5p in development of colorectal cancer (CRC) remain largely unknown. Transwell chambers were used to analyze effects on cell migration and invasion by miR-150-5p. Quantitative real-time PCR (qRT-PCR), Western blotting and dual-luciferase 3' UTR reporter assay were carried out to identify the target genes of miR-150-5p. In our research, miR-150-5p suppressed CRC cell migration and invasion, and MUC4 was identified as a direct target gene. Its effects were partly blocked by re-expression of MUC4. In conclusiomn, miR-150-5p may suppress CRC metastasis through directly targeting MUC4, highlighting its potential as a novel agent for the treatment of CRC metastasis.

Keywords

References

  1. Albrecht H, Carraway KL, 3rd (2011). MUC1 and MUC4: switching the emphasis from large to small. Cancer Biother Radiopharm, 26, 261-71. https://doi.org/10.1089/cbr.2011.1017
  2. Andrianifahanana M, Agrawal A, Singh AP, et al (2005). Synergistic induction of the MUC4 mucin gene by interferon-gamma and retinoic acid in human pancreatic tumour cells involves a reprogramming of signalling pathways. Oncogene, 24, 6143-54. https://doi.org/10.1038/sj.onc.1208756
  3. Arndt GM, Dossey L, Cullen LM, et al (2009). Characterization of global microRNA expression reveals oncogenic potential of miR-145 in metastatic colorectal cancer. BMC Cancer, 9, 374. https://doi.org/10.1186/1471-2407-9-374
  4. Audie JP, Janin A, Porchet N, et al (1993). Expression of human mucin genes in respiratory, digestive, and reproductive tracts ascertained by in situ hybridization. J Histochem Cytochem, 41, 1479-85. https://doi.org/10.1177/41.10.8245407
  5. Cao M, Hou D, Liang H, et al (2014). miR-150 promotes the proliferation and migration of lung cancer cells by targeting SRC kinase signalling inhibitor 1. Eur J Cancer, 50, 1013-24. https://doi.org/10.1016/j.ejca.2013.12.024
  6. Carraway KL, Perez A, Idris N, et al (2002). Muc4/sialomucin complex, the intramembrane ErbB2 ligand, in cancer and epithelia: to protect and to survive. Prog Nucleic Acid Res Mol Biol, 71, 149-85. https://doi.org/10.1016/S0079-6603(02)71043-X
  7. Chaturvedi P, Singh AP, Batra SK (2008). Structure, evolution, and biology of the MUC4 mucin. FASEB J, 22, 966-81.
  8. Chen HY, Lin YM, Chung HC, et al (2012). miR-103/107 promote metastasis of colorectal cancer by targeting the metastasis suppressors DAPK and KLF4. Cancer Res, 72, 3631-41. https://doi.org/10.1158/0008-5472.CAN-12-0667
  9. Corfield AP, Carroll D, Myerscough N, et al (2001). Mucins in the gastrointestinal tract in health and disease. Front Biosci, 6, 1321-57. https://doi.org/10.2741/Corfield
  10. Gao Y, Li BD, Liu YG (2013). Effect of miR27a on proliferation and invasion in colonic cancer cells. Asian Pac J Cancer Prev, 14, 4675-8. https://doi.org/10.7314/APJCP.2013.14.8.4675
  11. Huang S, Chen Y, Wu W, et al (2013). miR-150 promotes human breast cancer growth and malignant behavior by targeting the pro-apoptotic purinergic P2X7 receptor. PloS One, 8, 80707. https://doi.org/10.1371/journal.pone.0080707
  12. Jemal A, Siegel R, Ward E, et al (2009). Cancer statistics, 2009. CA Cancer J Clin, 59, 225-49. https://doi.org/10.3322/caac.20006
  13. Lahdaoui F, Delpu Y, Vincent A, et al (2014). miR-219-1-3p is a negative regulator of the mucin MUC4 expression and is a tumor suppressor in pancreatic cancer. Oncogene, 1-9.
  14. Lin YC, Kuo MW, Yu J, et al (2008). c-Myb is an evolutionary conserved miR-150 target and miR-150/c-Myb interaction is important for embryonic development. Mol Biol Evol, 25, 2189-98. https://doi.org/10.1093/molbev/msn165
  15. Ma Y, Zhang P, Wang F, et al (2012). miR-150 as a potential biomarker associated with prognosis and therapeutic outcome in colorectal cancer. Gut, 61, 1447-53. https://doi.org/10.1136/gutjnl-2011-301122
  16. Moniaux N, Chaturvedi P, Varshney GC, et al (2007). Human MUC4 mucin induces ultra-structural changes and tumorigenicity in pancreatic cancer cells. Br J Cancer, 97, 345-57. https://doi.org/10.1038/sj.bjc.6603868
  17. Mukhopadhyay P, Lakshmanan I, Ponnusamy MP, et al (2013). MUC4 overexpression augments cell migration and metastasis through EGFR family proteins in triple negative breast cancer cells. PloS One, 8, 54455. https://doi.org/10.1371/journal.pone.0054455
  18. Ogata-Kawata H, Izumiya M, Kurioka D, et al (2014). Circulating Exosomal microRNAs as Biomarkers of Colon Cancer. PloS One, 9, 92921. https://doi.org/10.1371/journal.pone.0092921
  19. Perrais M, Pigny P, Ducourouble MP, et al (2001). Characterization of human mucin gene MUC4 promoter: importance of growth factors and proinflammatory cytokines for its regulation in pancreatic cancer cells. J Biol Chem, 276, 30923-33. https://doi.org/10.1074/jbc.M104204200
  20. Pizzini S, Bisognin A, Mandruzzato S, et al (2013). Impact of microRNAs on regulatory networks and pathways in human colorectal carcinogenesis and development of metastasis. BMC Genomics, 14, 589-602. https://doi.org/10.1186/1471-2164-14-589
  21. Ponnusamy MP, Singh AP, Jain M, et al (2008). MUC4 activates HER2 signalling and enhances the motility of human ovarian cancer cells. Br J Cancer, 99, 520-6. https://doi.org/10.1038/sj.bjc.6604517
  22. Rachagani S, Macha MA, Ponnusamy MP, et al (2012). MUC4 potentiates invasion and metastasis of pancreatic cancer cells through stabilization of fibroblast growth factor receptor 1. Carcinogenesis, 33, 1953-64. https://doi.org/10.1093/carcin/bgs225
  23. Shanmugam C, Jhala NC, Katkoori VR, et al (2010). Prognostic value of mucin 4 expression in colorectal adenocarcinomas. Cancer, 116, 3577-86. https://doi.org/10.1002/cncr.25095
  24. Srivastava SK, Bhardwaj A, Singh S, et al (2011). MicroRNA-150 directly targets MUC4 and suppresses growth and malignant behavior of pancreatic cancer cells. Carcinogenesis, 32, 1832-9. https://doi.org/10.1093/carcin/bgr223
  25. Tang W, Zhu Y, Gao J, et al (2014). MicroRNA-29a promotes colorectal cancer metastasis by regulating matrix metalloproteinase 2 and E-cadherin via KLF4. Br J Cancer, 110, 450-8. https://doi.org/10.1038/bjc.2013.724
  26. Vincent A, Ducourouble MP, Van Seuningen I (2008). Epigenetic regulation of the human mucin gene MUC4 in epithelial cancer cell lines involves both DNA methylation and histone modifications mediated by DNA methyltransferases and histone deacetylases. FASEB J, 22, 3035-45. https://doi.org/10.1096/fj.07-103390
  27. Wang CJ, Stratmann J, Zhou ZG, et al (2010). Suppression of microRNA-31 increases sensitivity to 5-FU at an early stage, and affects cell migration and invasion in HCT-116 colon cancer cells. BMC Cancer, 10, 616-28. https://doi.org/10.1186/1471-2407-10-616
  28. Watanabe A, Tagawa H, Yamashita J, et al (2011). The role of microRNA-150 as a tumor suppressor in malignant lymphoma. Leukemia, 25, 1324-34. https://doi.org/10.1038/leu.2011.81
  29. Wu Q, Jin H, Yang Z, et al (2010). MiR-150 promotes gastric cancer proliferation by negatively regulating the proapoptotic gene EGR2. Biochem Biophys Res Commun, 392, 340-5. https://doi.org/10.1016/j.bbrc.2009.12.182
  30. Zhang J, Xiao Z, Lai D, et al (2012). miR-21, miR-17 and miR-19a induced by phosphatase of regenerating liver-3 promote the proliferation and metastasis of colon cancer. Br J Cancer, 107, 352-9. https://doi.org/10.1038/bjc.2012.251

Cited by

  1. MiR-1297 Regulates the Growth, Migration and Invasion of Colorectal Cancer Cells by Targeting Cyclo-oxygenase-2 vol.15, pp.21, 2014, https://doi.org/10.7314/APJCP.2014.15.21.9185
  2. miR-150-5p Inhibits Hepatoma Cell Migration and Invasion by Targeting MMP14 vol.9, pp.12, 2014, https://doi.org/10.1371/journal.pone.0115577
  3. Downregulation of OGDHL expression is associated with promoter hypermethylation in colorectal cancer vol.49, pp.4, 2015, https://doi.org/10.1134/S0026893315040044
  4. Profiling of downregulated blood-circulating miR-150-5p as a novel tumor marker for cholangiocarcinoma vol.37, pp.11, 2016, https://doi.org/10.1007/s13277-016-5313-6
  5. Identification of lymph node metastasis-related microRNAs in lung adenocarcinoma and analysis of the underlying mechanisms using a bioinformatics approach vol.242, pp.7, 2017, https://doi.org/10.1177/1535370216677353
  6. The Role of MicroRNAs in the Chemopreventive Activity of Sulforaphane from Cruciferous Vegetables vol.9, pp.8, 2017, https://doi.org/10.3390/nu9080902
  7. MicroRNA-150 targets Rho-associated protein kinase 1 to inhibit cell proliferation, migration and invasion in papillary thyroid carcinoma vol.16, pp.2, 2017, https://doi.org/10.3892/mmr.2017.6842
  8. mutation in papillary thyroid cancer cells vol.119, pp.11, 2018, https://doi.org/10.1002/jcb.27108