Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2015 (2015), Article ID 823620, 12 pages
http://dx.doi.org/10.1155/2015/823620
Review Article

MicroRNAs as Regulator of Signaling Networks in Metastatic Colon Cancer

1Human Stem Cell Institute of the General Hospital, Ningxia Medical University, Yinchuan 750004, China
2Department of Colorectal Surgery, The General Hospital of Ningxia Medical University, Yinchuan 750004, China
3Department of Clinical Oncology, Queen Elizabeth Hospital, Kowloon, Hong Kong

Received 2 February 2015; Revised 6 April 2015; Accepted 6 April 2015

Academic Editor: Yun Yen

Copyright © 2015 Jian Wang et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. Ferlay, H.-R. Shin, F. Bray, D. Forman, C. Mathers, and D. M. Parkin, “Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008,” International Journal of Cancer, vol. 127, no. 12, pp. 2893–2917, 2010. View at Publisher · View at Google Scholar · View at Scopus
  2. J. Fritzmann, M. Morkel, D. Besser et al., “A colorectal cancer expression profile that includes transforming growth factor β inhibitor BAMBI predicts metastatic potential,” Gastroenterology, vol. 137, no. 1, pp. 165–175, 2009. View at Publisher · View at Google Scholar · View at Scopus
  3. J. Han, Y. Lee, K.-H. Yeom, Y.-K. Kim, H. Jin, and V. N. Kim, “The Drosha-DGCR8 complex in primary microRNA processing,” Genes and Development, vol. 18, no. 24, pp. 3016–3027, 2004. View at Publisher · View at Google Scholar · View at Scopus
  4. J. Manikandan, J. J. Aarthi, S. D. Kumar, and P. N. Pushparaj, “Oncomirs: the potential role of non-coding microRNAs in understanding cancer,” Bioinformation, vol. 2, no. 8, pp. 330–334, 2008. View at Publisher · View at Google Scholar
  5. K. Schee, Ø. Fodstad, and K. Flatmark, “MicroRNAs as biomarkers in colorectal cancer,” The American Journal of Pathology, vol. 177, no. 4, pp. 1592–1599, 2010. View at Publisher · View at Google Scholar · View at Scopus
  6. G. di Leva, M. Garofalo, and C. M. Croce, “MicroRNAs in cancer,” Annual Review of Pathology, vol. 9, pp. 287–314, 2014. View at Publisher · View at Google Scholar · View at Scopus
  7. S. Muhammad, K. Kaur, R. Huang et al., “MicroRNAs in colorectal cancer: role in metastasis and clinical perspectives,” World Journal of Gastroenterology, vol. 20, no. 45, pp. 17011–17019, 2014. View at Publisher · View at Google Scholar
  8. K. Hur, Y. Toiyama, M. Takahashi et al., “MicroRNA-200c modulates epithelial-tomesenchymal transition (EMT) in human colorectal cancer metastasis,” Gut, vol. 62, no. 9, pp. 1315–1326, 2013. View at Publisher · View at Google Scholar · View at Scopus
  9. L. Hong, Y. Han, J. Yang et al., “MicroRNAs in gastrointestinal cancer: prognostic significance and potential role in chemoresistance,” Expert Opinion on Biological Therapy, vol. 14, no. 8, pp. 1103–1111, 2014. View at Publisher · View at Google Scholar
  10. D. Hanahan and R. A. Weinberg, “Hallmarks of cancer: the next generation,” Cell, vol. 144, no. 5, pp. 646–674, 2011. View at Publisher · View at Google Scholar · View at Scopus
  11. A. Bonauer, G. Carmona, M. Iwasaki et al., “MicroRNA-92a controls angiogenesis and functional recovery of ischemic tissues in mice,” Science, vol. 324, no. 5935, pp. 1710–1713, 2009. View at Publisher · View at Google Scholar · View at Scopus
  12. T. Ota, K. Doi, T. Fujimoto et al., “KRAS up-regulates the expression of miR-181a, miR-200c and miR-210 in a three-dimensional-specific manner in DLD-1 colorectal cancer cells,” Anticancer Research, vol. 32, no. 6, pp. 2271–2276, 2012. View at Google Scholar · View at Scopus
  13. S. T. Guo, C. C. Jiang, G. P. Wang et al., “MicroRNA-497 targets insulin-like growth factor 1 receptor and has a tumour suppressive role in human colorectal cancer,” Oncogene, vol. 32, no. 15, pp. 1910–1920, 2013. View at Publisher · View at Google Scholar · View at Scopus
  14. L. W. Dobrucki, Y. Tsutsumi, L. Kalinowski et al., “Analysis of angiogenesis induced by local IGF-1 expression after myocardial infarction using microSPECT-CT imaging,” Journal of Molecular and Cellular Cardiology, vol. 48, no. 6, pp. 1071–1079, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. K. H. Chang, N. Miller, E. A. H. Kheirelseid et al., “MicroRNA signature analysis in colorectal cancer: identification of expression profiles in stage II tumors associated with aggressive disease,” International Journal of Colorectal Disease, vol. 26, no. 11, pp. 1415–1422, 2011. View at Publisher · View at Google Scholar · View at Scopus
  16. H.-Y. Chen, Y.-M. Lin, H.-C. Chung et al., “MiR-103/107 promote metastasis of colorectal cancer by targeting the metastasis suppressors DAPK and KLF4,” Cancer Research, vol. 72, no. 14, pp. 3631–3641, 2012. View at Publisher · View at Google Scholar · View at Scopus
  17. J. Fu, W. Tang, P. Du et al., “Identifying MicroRNA-mRNA regulatory network in colorectal cancer by a combination of expression profile and bioinformatics analysis,” BMC Systems Biology, vol. 6, article 68, 2012. View at Publisher · View at Google Scholar · View at Scopus
  18. P. Tokarz and J. Blasiak, “The role of microRNA in metastatic colorectal cancer and its significance in cancer prognosis and treatment,” Acta Biochimica Polonica, vol. 59, no. 4, pp. 467–474, 2012. View at Google Scholar · View at Scopus
  19. Z. Sun, Z. Zhang, Z. Liu, B. Qiu, K. Liu, and G. Dong, “MicroRNA-335 inhibits invasion and metastasis of colorectal cancer by targeting ZEB2,” Medical Oncology, vol. 31, no. 6, 2014. View at Publisher · View at Google Scholar · View at Scopus
  20. J. Kim, N. J. Lim, S. G. Jang, H. K. Kim, and G. K. Lee, “miR-592 and miR-552 can distinguish between primary lung adenocarcinoma and colorectal cancer metastases in the lung,” Anticancer Research, vol. 34, no. 5, pp. 2297–2302, 2014. View at Google Scholar
  21. Y. Sun, S. Shen, X. Liu et al., “MiR-429 inhibits cells growth and invasion and regulates EMT-related marker genes by targeting Onecut2 in colorectal carcinoma,” Molecular and Cellular Biochemistry, vol. 390, no. 1-2, pp. 19–30, 2014. View at Publisher · View at Google Scholar · View at Scopus
  22. L.-F. Lu and A. Liston, “MicroRNA in the immune system, microRNA as an immune system,” Immunology, vol. 127, no. 3, pp. 291–298, 2009. View at Publisher · View at Google Scholar · View at Scopus
  23. E. Penna, F. Orso, D. Cimino et al., “MicroRNA-214 contributes to melanoma tumour progression through suppression of TFAP2C,” EMBO Journal, vol. 30, no. 10, pp. 1990–2007, 2011. View at Publisher · View at Google Scholar · View at Scopus
  24. M. M. Vickers, J. Bar, I. Gorn-Hondermann et al., “Stage-dependent differential expression of microRNAs in colorectal cancer: potential role as markers of metastatic disease,” Clinical and Experimental Metastasis, vol. 29, no. 2, pp. 123–132, 2012. View at Publisher · View at Google Scholar · View at Scopus
  25. J. D. Hudson, M. A. Shoaibi, R. Maestro, A. Carnero, G. J. Hannon, and D. H. Beach, “A proinflammatory cytokine inhibits p53 tumor suppressor activity,” Journal of Experimental Medicine, vol. 190, no. 10, pp. 1375–1382, 1999. View at Publisher · View at Google Scholar · View at Scopus
  26. Y.-L. Ma, P. Zhang, F. Wang et al., “Human embryonic stem cells and metastatic colorectal cancer cells shared the common endogenous human microRNA-26b,” Journal of Cellular and Molecular Medicine, vol. 15, no. 9, pp. 1941–1954, 2011. View at Publisher · View at Google Scholar · View at Scopus
  27. Y. Yu, S. S. Kanwar, B. B. Patel et al., “MicroRNA-21 induces stemness by downregulating transforming growth factor beta receptor 2 (TGFbetaR2) in colon cancer cells,” Carcinogenesis, vol. 33, no. 1, pp. 68–76, 2012. View at Publisher · View at Google Scholar · View at Scopus
  28. S.-Y. Ju, S.-H. Chiou, and Y. Su, “Maintenance of the stemness in CD44+ HCT-15 and HCT-116 human colon cancer cells requires miR-203 suppression,” Stem Cell Research, vol. 12, no. 1, pp. 86–100, 2014. View at Publisher · View at Google Scholar · View at Scopus
  29. F. Sipos and O. Galamb, “Epithelial-to-mesenchymal and mesenchymal-to-epithelial transitions in the colon,” World Journal of Gastroenterology, vol. 18, no. 7, pp. 601–608, 2012. View at Publisher · View at Google Scholar · View at Scopus
  30. C. L. Cottonham, S. Kaneko, and L. Xu, “miR-21 and miR-31 converge on TIAM1 to regulate migration and invasion of colon carcinoma cells,” The Journal of Biological Chemistry, vol. 285, no. 46, pp. 35293–35302, 2010. View at Publisher · View at Google Scholar · View at Scopus
  31. L. Shi, R. Jackstadt, H. Siemens, H. Li, T. Kirchner, and H. Hermeking, “P53-induced miR-15a/16-1 and AP4 form a double-negative feedback loop to regulate epithelial-mesenchymal transition and metastasis in colorectal cancer,” Cancer Research, vol. 74, no. 2, pp. 532–542, 2014. View at Publisher · View at Google Scholar · View at Scopus
  32. C. G. Lee, S. McCarthy, M. Gruidl, C. Timme, and T. J. Yeatman, “MicroRNA-147 induces a mesenchymal-to-epithelial transition (MET) and reverses EGFR inhibitor resistance,” PLoS ONE, vol. 9, no. 1, Article ID e84597, 2014. View at Publisher · View at Google Scholar · View at Scopus
  33. J. B. Kjersem, T. Ikdahl, O. C. Lingjaerde, T. Guren, K. M. Tveit, and E. H. Kure, “Plasma microRNAs predicting clinical outcome in metastatic colorectal cancer patients receiving first-line oxaliplatin-based treatment,” Molecular Oncology, vol. 8, no. 1, pp. 59–67, 2014. View at Publisher · View at Google Scholar · View at Scopus
  34. H. Ogata-Kawata, M. Izumiya, D. Kurioka et al., “Circulating exosomal microRNAs as biomarkers of colon cancer,” PLoS ONE, vol. 9, no. 4, Article ID e92921, 2014. View at Publisher · View at Google Scholar · View at Scopus
  35. O. Slaby, M. Svoboda, J. Michalek, and R. Vyzula, “MicroRNAs in colorectal cancer,” in MicroRNAs in Cancer Translational Research, W. C. Cho, Ed., pp. 107–133, Springer, Dordrecht, The Netherlands, 2011. View at Google Scholar
  36. C. Kantara, M. R. O'Connell, G. Luthra et al., “Methods for detecting circulating cancer stem cells (CCSCs) as a novel approach for diagnosis of colon cancer relapse/metastasis,” Laboratory Investigation, vol. 95, no. 1, pp. 100–112, 2014. View at Publisher · View at Google Scholar
  37. J. E. Fish, M. M. Santoro, S. U. Morton et al., “miR-126 regulates angiogenic signaling and vascular integrity,” Developmental Cell, vol. 15, no. 2, pp. 272–284, 2008. View at Publisher · View at Google Scholar · View at Scopus
  38. S. Rodriguez and U. Huynh-Do, “The role of PTEN in tumor angiogenesis,” Journal of Oncology, vol. 2012, Article ID 141236, 11 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  39. M. Dews, A. Homayouni, D. Yu et al., “Augmentation of tumor angiogenesis by a Myc-activated microRNA cluster,” Nature Genetics, vol. 38, no. 9, pp. 1060–1065, 2006. View at Publisher · View at Google Scholar · View at Scopus
  40. L. Fang, H. Li, L. Wang et al., “MicroRNA-17-5p promotes chemotherapeutic drug resistance and tumour metastasis of colorectal cancer by repressing PTEN expression,” Oncotarget, vol. 5, no. 10, pp. 2974–2987, 2014. View at Google Scholar
  41. W. Wu, J. Yang, X. Feng et al., “MicroRNA-32 (miR-32) regulates phosphatase and tensin homologue (PTEN) expression and promotes growth, migration, and invasion in colorectal carcinoma cells,” Molecular Cancer, vol. 12, no. 1, article 30, 2013. View at Publisher · View at Google Scholar · View at Scopus
  42. N. Li, A. Tang, S. Huang et al., “MiR-126 suppresses colon cancer cell proliferation and invasion via inhibiting RhoA/ROCK signaling pathway,” Molecular and Cellular Biochemistry, vol. 380, no. 1-2, pp. 107–119, 2013. View at Publisher · View at Google Scholar · View at Scopus
  43. C. Faber, T. Kirchner, and F. Hlubek, “The impact of microRNAs on colorectal cancer,” Virchows Archiv, vol. 454, no. 4, pp. 359–367, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. G. G. Gomez, J. Wykosky, C. Zanca, F. B. Furnari, and W. K. Cavenee, “Therapeutic resistance in cancer: microRNA regulation of EGFR signaling networks,” Cancer Biology and Medicine, vol. 10, no. 4, pp. 192–205, 2013. View at Publisher · View at Google Scholar · View at Scopus
  45. R. Giampieri, M. Scartozzi, M. del Prete et al., “Molecular biomarkers of resistance to anti-EGFR treatment in metastatic colorectal cancer, from classical to innovation,” Critical Reviews in Oncology/Hematology, vol. 88, no. 2, pp. 272–283, 2013. View at Publisher · View at Google Scholar · View at Scopus
  46. A. Deyati, S. Bagewadi, P. Senger, M. Hofmann-Apitius, and N. Novac, “Systems approach for the selection of micro-RNAs as therapeutic biomarkers of anti-EGFR monoclonal antibody treatment in colorectal cancer,” Scientific Reports, vol. 5, article 8013, 2015. View at Publisher · View at Google Scholar
  47. T. Suto, T. Yokobori, R. Yajima et al., “MicroRNA-7 expression in colorectal cancer is associated with poor prognosis and regulates cetuximab sensitivity via EGFR regulation,” Carcinogenesis, vol. 36, no. 3, pp. 338–345, 2015. View at Publisher · View at Google Scholar
  48. J. Mlcochova, P. Faltejskova, R. Nemecek, M. Svoboda, and O. Slaby, “MicroRNAs targeting EGFR signalling pathway in colorectal cancer,” Journal of Cancer Research and Clinical Oncology, vol. 139, no. 10, pp. 1615–1624, 2013. View at Publisher · View at Google Scholar · View at Scopus
  49. F. Cappuzzo, A. Sacconi, L. Landi et al., “MicroRNA signature in metastatic colorectal cancer patients treated with anti-EGFR monoclonal antibodies,” Clinical Colorectal Cancer, vol. 13, no. 1, pp. 37–45.e4, 2014. View at Publisher · View at Google Scholar · View at Scopus
  50. A. Ruzzo, F. Graziano, B. Vincenzi et al., “High let-7a microRNA levels in KRAS-mutated colorectal carcinomas may rescue anti-EGFR therapy effects in patients with chemotherapy-refractory metastatic disease,” The Oncologist, vol. 17, no. 6, pp. 823–829, 2012. View at Publisher · View at Google Scholar · View at Scopus
  51. M. Pichler, E. Winter, A. L. Ress et al., “MiR-181a is associated with poor clinical outcome in patients with colorectal cancer treated with EGFR inhibitor,” Journal of Clinical Pathology, vol. 67, no. 3, pp. 198–203, 2014. View at Publisher · View at Google Scholar · View at Scopus
  52. G. Manceau, S. Imbeaud, R. Thiebaut et al., “Hsa-miR-31-3p expression is linked to progression-free survival in patients with KRAS wild-type metastatic colorectal cancer treated with anti-EGFR therapy,” Clinical Cancer Research, vol. 20, no. 12, pp. 3338–3347, 2014. View at Publisher · View at Google Scholar
  53. D. Ji, Z. Chen, M. Li et al., “MicroRNA-181a promotes tumor growth and liver metastasis in colorectal cancer by targeting the tumor suppressor WIF-1,” Molecular Cancer, vol. 13, article 86, 2014. View at Publisher · View at Google Scholar · View at Scopus
  54. H. Butz, K. Rácz, L. Hunyady, and A. Patócs, “Crosstalk between TGF-β signaling and the microRNA machinery,” Trends in Pharmacological Sciences, vol. 33, no. 7, pp. 382–393, 2012. View at Publisher · View at Google Scholar · View at Scopus
  55. M. Korpal, E. S. Lee, G. Hu, and Y. Kang, “The miR-200 family inhibits epithelial-mesenchymal transition and cancer cell migration by direct targeting of E-cadherin transcriptional repressors ZEB1 and ZEB2,” The Journal of Biological Chemistry, vol. 283, no. 22, pp. 14910–14914, 2008. View at Publisher · View at Google Scholar · View at Scopus
  56. M. Rokavec, H. Li, L. Jiang et al., “The p53/microRNA connection in gastrointestinal cancer,” Clinical and Experimental Gastroenterology, vol. 7, pp. 395–413, 2014. View at Google Scholar
  57. A. Pagliuca, C. Valvo, E. Fabrizi et al., “Analysis of the combined action of miR-143 and miR-145 on oncogenic pathways in colorectal cancer cells reveals a coordinate program of gene repression,” Oncogene, vol. 32, no. 40, pp. 4806–4813, 2013. View at Publisher · View at Google Scholar · View at Scopus
  58. P. Bu, K.-Y. Chen, J. H. Chen et al., “A microRNA miR-34a-regulated bimodal switch targets notch in colon cancer stem cells,” Cell Stem Cell, vol. 12, no. 5, pp. 602–615, 2013. View at Publisher · View at Google Scholar · View at Scopus
  59. J. Pekow, K. Meckel, U. Dougherty et al., “Tumor suppressors miR-143 and miR-145 and predicted target proteins API5, ERK5, K-RAS, and IRS-1 are differentially expressed in proximal and distal colon,” The American Journal of Physiology—Gastrointestinal and Liver Physiology, vol. 308, no. 3, pp. G179–G187, 2015. View at Publisher · View at Google Scholar
  60. G. M. Arndt, L. Dossey, L. M. Cullen et al., “Characterization of global microRNA expression reveals oncogenic potential of miR-145 in metastatic colorectal cancer,” BMC Cancer, vol. 9, article 374, 2009. View at Publisher · View at Google Scholar · View at Scopus
  61. Y. Fang, X. Gu, Z. Li, J. Xiang, and Z. Chen, “miR-449b inhibits the proliferation of SW1116 colon cancer stem cells through downregulation of CCND1 and E2F3 expression,” Oncology Reports, vol. 30, no. 1, pp. 399–406, 2013. View at Publisher · View at Google Scholar · View at Scopus
  62. M. Niyazi, F. Zehentmayr, O. M. Niemöller et al., “MiRNA expression patterns predict survival in glioblastoma,” Radiation Oncology, vol. 6, no. 1, article 153, 2011. View at Publisher · View at Google Scholar · View at Scopus
  63. N. Mencia, E. Selga, V. Noé, and C. J. Ciudad, “Underexpression of miR-224 in methotrexate resistant human colon cancer cells,” Biochemical Pharmacology, vol. 82, no. 11, pp. 1572–1582, 2011. View at Publisher · View at Google Scholar · View at Scopus
  64. B. Song, Y. Wang, M. A. Titmus et al., “Molecular mechanism of chemoresistance by miR-215 in osteosarcoma and colon cancer cells,” Molecular Cancer, vol. 9, article 96, 2010. View at Publisher · View at Google Scholar · View at Scopus
  65. X. Li, H. Zhao, X. Zhou, and L. Song, “Inhibition of lactate dehydrogenase A by microRNA-34a resensitizes colon cancer cells to 5-fluorouracil,” Molecular Medicine Reports, vol. 11, no. 1, pp. 577–582, 2014. View at Publisher · View at Google Scholar
  66. Y. Zhang, L. Geng, G. Talmon, and J. Wang, “MicroRNA-520g confers drug resistance by regulating p21 expression in colorectal cancer,” The Journal of Biological Chemistry, vol. 290, no. 10, pp. 6215–6225, 2015. View at Publisher · View at Google Scholar
  67. A. Weissmann-Brenner, M. Kushnir, G. L. Yanai et al., “Tumor microRNA-29a expression and the risk of recurrence in stage II colon cancer,” International Journal of Oncology, vol. 40, no. 6, pp. 2097–2103, 2012. View at Publisher · View at Google Scholar · View at Scopus
  68. J. Yin, Z. Bai, J. Song et al., “Differential expression of serum miR-126, miR-141 and miR-21 as novel biomarkers for early detection of liver metastasis in colorectal cancer,” Chinese Journal of Cancer Research, vol. 26, no. 1, pp. 95–103, 2014. View at Publisher · View at Google Scholar · View at Scopus
  69. M. Fujiya, H. Konishi, M. K. M. Kamel et al., “microRNA-18a induces apoptosis in colon cancer cells via the autophagolysosomal degradation of oncogenic heterogeneous nuclear ribonucleoprotein A1,” Oncogene, vol. 33, no. 40, pp. 4847–4856, 2013. View at Publisher · View at Google Scholar · View at Scopus
  70. J. Xing, S. Wan, F. Zhou et al., “Genetic polymorphisms in pre-microRNA genes as prognostic markers of colorectal cancer,” Cancer Epidemiology Biomarkers and Prevention, vol. 21, no. 1, pp. 217–227, 2012. View at Publisher · View at Google Scholar · View at Scopus
  71. P. F. Engstrom, J. P. Arnoletti, A. B. Benson III et al., “NCCN clinical practice guidelines in oncology: colon cancer,” Journal of the National Comprehensive Cancer Network, vol. 7, no. 8, pp. 778–831, 2009. View at Google Scholar
  72. A. J. Schetter, S. Y. Leung, J. J. Sohn et al., “MicroRNA expression profiles associated with prognosis and therapeutic outcome in colon adenocarcinoma,” Journal of the American Medical Association, vol. 299, no. 4, pp. 425–436, 2008. View at Publisher · View at Google Scholar · View at Scopus
  73. N. Valeri, P. Gasparini, C. Braconi et al., “MicroRNA-21 induces resistance to 5-fluorouracil by down-regulating human DNA MutS homolog 2 (hMSH2),” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 49, pp. 21098–21103, 2010. View at Publisher · View at Google Scholar · View at Scopus
  74. K. Bakirtzi, M. Hatziapostolou, I. Karagiannides et al., “Neurotensin signaling activates microRNAs-21 and -155 and Akt, promotes tumor growth in mice, and is increased in human colon tumors,” Gastroenterology, vol. 141, no. 5, pp. 1749.e1–1761.e1, 2011. View at Publisher · View at Google Scholar · View at Scopus
  75. G. Nakajima, K. Hayashi, Y. Xi et al., “Non-coding microRNAs hsa-let-7g and hsa-miR-181b are associated with chemoresponse to S-1 in colon cancer,” Cancer Genomics and Proteomics, vol. 3, no. 5, pp. 317–324, 2006. View at Google Scholar · View at Scopus
  76. F. Ebrahimi, V. Gopalan, R. A. Smith, and A. K.-Y. Lam, “MiR-126 in human cancers: clinical roles and current perspectives,” Experimental and Molecular Pathology, vol. 96, no. 1, pp. 98–107, 2014. View at Publisher · View at Google Scholar · View at Scopus
  77. C. Guo, J. F. Sah, L. Beard, J. K. V. Willson, S. D. Markowitz, and K. Guda, “The noncoding RNA, miR-126, suppresses the growth of neoplastic cells by targeting phosphatidylinositol 3-kinase signaling and is frequently lost in colon cancers,” Genes Chromosomes and Cancer, vol. 47, no. 11, pp. 939–946, 2008. View at Publisher · View at Google Scholar · View at Scopus
  78. X. T. Xu, Q. Xu, J. L. Tong et al., “MicroRNA expression profiling identifies miR-328 regulates cancer stem cell-like SP cells in colorectal cancer,” British Journal of Cancer, vol. 106, no. 7, pp. 1320–1330, 2012. View at Publisher · View at Google Scholar · View at Scopus
  79. Y.-Y. Qiu, Q. Hu, Q.-F. Tang et al., “MicroRNA-497 and bufalin act synergistically to inhibit colorectal cancer metastasis,” Tumor Biology, vol. 35, no. 3, pp. 2599–2606, 2014. View at Publisher · View at Google Scholar · View at Scopus
  80. V. Stiegelbauer, S. Perakis, A. Deutsch, and et al, “MicroRNAs as novel predictive biomarkers and therapeutic targets in colorectal cancer,” World Journal of Gastroenterology, vol. 20, no. 33, pp. 11727–11735, 2014. View at Publisher · View at Google Scholar
  81. H. W. Yu and W. C. Cho, “The emerging role of miRNAs in combined cancer therapy,” Expert Opinion on Biological Therapy, 2015. View at Publisher · View at Google Scholar
  82. F. Wang, S. C. C. Wong, L. W. C. Chan, W. C. S. Cho, S. P. Yip, and B. Y. M. Yung, “Multiple regression analysis of mRNA-miRNA associations in colorectal cancer pathway,” BioMed Research International, vol. 2014, Article ID 676724, 8 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  83. K. Motoyama, H. Inoue, Y. Nakamura, H. Uetake, K. Sugihara, and M. Mori, “Clinical significance of high mobility group A2 in human gastric cancer and its relationship to let-7 MicroRNA family,” Clinical Cancer Research, vol. 14, no. 8, pp. 2334–2340, 2008. View at Publisher · View at Google Scholar · View at Scopus
  84. S. M. Johnson, H. Grosshans, J. Shingara et al., “RAS is regulated by the let-7 microRNA family,” Cell, vol. 120, no. 5, pp. 635–647, 2005. View at Publisher · View at Google Scholar · View at Scopus
  85. A. Strillacci, C. Griffoni, P. Sansone et al., “MiR-101 downregulation is involved in cyclooxygenase-2 overexpression in human colon cancer cells,” Experimental Cell Research, vol. 315, no. 8, pp. 1439–1447, 2009. View at Publisher · View at Google Scholar · View at Scopus
  86. Y. Ueda, T. Ando, S. Nanjo, T. Ushijima, and T. Sugiyama, “DNA methylation of microRNA-124a is a potential risk marker of colitis-associated cancer in patients with ulcerative colitis,” Digestive Diseases and Sciences, vol. 59, no. 10, pp. 2444–2451, 2014. View at Publisher · View at Google Scholar · View at Scopus
  87. C. W. Lin, X. R. Li, Y. Zhang et al., “TAp63 suppress metastasis via miR-133b in colon cancer cells,” British Journal of Cancer, vol. 110, no. 9, pp. 2310–2320, 2014. View at Publisher · View at Google Scholar · View at Scopus
  88. F. Balaguer, A. Link, J. J. Lozano et al., “Epigenetic silencing of miR-137 is an early event in colorectal carcinogenesis,” Cancer Research, vol. 70, no. 16, pp. 6609–6618, 2010. View at Publisher · View at Google Scholar · View at Scopus
  89. C. J. Braun, X. Zhang, I. Savelyeva et al., “p53-responsive microRNAs 192 and 215 are capable of inducing cell cycle arrest,” Cancer Research, vol. 68, no. 24, pp. 10094–10104, 2008. View at Publisher · View at Google Scholar · View at Scopus
  90. X. Meng, J. Wu, C. Pan et al., “Genetic and epigenetic down-regulation of microRNA-212 promotes colorectal tumor metastasis via dysregulation of MnSOD,” Gastroenterology, vol. 145, no. 2, pp. 426.e6–436.e6, 2013. View at Publisher · View at Google Scholar · View at Scopus
  91. Y. Bao, Z. Chen, Y. Guo et al., “Tumor suppressor microRNA-27a in colorectal carcinogenesis and progression by targeting SGPP1 and Smad2,” PLoS ONE, vol. 9, no. 8, 2014. View at Publisher · View at Google Scholar
  92. J. He, G. Xie, J. Tong et al., “Overexpression of microRNA-122 re-sensitizes 5-FU-resistant colon cancer cells to 5-FU through the inhibition of PKM2 in vitro and in vivo,” Cell Biochemistry and Biophysics, vol. 70, no. 2, pp. 1343–1350, 2014. View at Publisher · View at Google Scholar · View at Scopus
  93. I. Iino, H. Kikuchi, S. Miyazaki et al., “Effect of miR-122 and its target gene cationic amino acid transporter 1 on colorectal liver metastasis,” Cancer Science, vol. 104, no. 5, pp. 624–630, 2013. View at Publisher · View at Google Scholar · View at Scopus
  94. S. Rossi, A. F. Di Narzo, P. Mestdagh et al., “MicroRNAs in colon cancer: a roadmap for discovery,” FEBS Letters, vol. 586, no. 19, pp. 3000–3007, 2012. View at Publisher · View at Google Scholar · View at Scopus
  95. S. Pizzini, A. Bisognin, S. Mandruzzato et al., “Impact of microRNAs on regulatory networks and pathways in human colorectal carcinogenesis and development of metastasis,” BMC Genomics, vol. 14, no. 1, article 589, 2013. View at Publisher · View at Google Scholar · View at Scopus
  96. Y. Zhang, X. Wang, Z. Wang, H. Tang, H. Fan, and Q. Guo, “miR-182 promotes cell growth and invasion by targeting forkhead box F2 transcription factor in colorectal cancer,” Oncology Reports, vol. 33, no. 5, pp. 2592–2598, 2015. View at Publisher · View at Google Scholar
  97. Y. Sun, X. Xing, Q. Liu et al., “Hypoxia-induced autophagy reduces radiosensitivity by the HIF-1alpha/miR-210/Bcl-2 pathway in colon cancer cells,” International Journal of Oncology, vol. 46, no. 2, pp. 750–756, 2015. View at Publisher · View at Google Scholar
  98. D. Liu, C. Liu, X. Wang, S. Ingvarsson, and H. Chen, “MicroRNA-451 suppresses tumor cell growth by down-regulating IL6R gene expression,” Cancer Epidemiology, vol. 38, no. 1, pp. 85–92, 2014. View at Publisher · View at Google Scholar · View at Scopus
  99. W. P. Tsang, E. K. O. Ng, S. S. M. Ng et al., “Oncofetal H19-derived miR-675 regulates tumor suppressor RB in human colorectal cancer,” Carcinogenesis, vol. 31, no. 3, pp. 350–358, 2010. View at Publisher · View at Google Scholar · View at Scopus
  100. S. Shell, S.-M. Park, A. R. Radjabi et al., “Let-7 expression defines two differentiation stages of cancer,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 27, pp. 11400–11405, 2007. View at Publisher · View at Google Scholar · View at Scopus
  101. R. Khatri and S. Subramanian, “MicroRNA-135b and its circuitry networks as potential therapeutic targets in colon cancer,” Frontiers in Oncology, vol. 3, article 268, 2013. View at Google Scholar
  102. N. Valeri, C. Braconi, P. Gasparini et al., “MicroRNA-135b promotes cancer progression by acting as a downstream effector of oncogenic pathways in colon cancer,” Cancer Cell, vol. 25, no. 4, pp. 469–483, 2014. View at Publisher · View at Google Scholar · View at Scopus
  103. T. Iwaya, T. Yokobori, N. Nishida et al., “Downregulation of miR-144 is associated with colorectal cancer progression via activation of mTOR signaling pathway,” Carcinogenesis, vol. 33, no. 12, Article ID bgs288, pp. 2391–2397, 2012. View at Publisher · View at Google Scholar · View at Scopus
  104. Z. J. Lu, L. G. Lu, K. Z. Tao et al., “MicroRNA-185 suppresses growth and invasion of colon cancer cells through inhibition of the hypoxiainducible factor-2alpha pathway in vitro and in vivo,” Molecular Medicine Reports, vol. 10, no. 5, pp. 2401–2408, 2014. View at Google Scholar
  105. C. C. Schimanski, K. Frerichs, F. Rahman et al., “High miR-196a levels promote the oncogenic phenotype of colorectal cancer cells,” World Journal of Gastroenterology, vol. 15, no. 17, pp. 2089–2096, 2009. View at Publisher · View at Google Scholar · View at Scopus
  106. J. Wu, G. Wu, L. Lv et al., “MicroRNA-34a inhibits migration and invasion of colon cancer cells via targeting to Fra-1,” Carcinogenesis, vol. 33, no. 3, pp. 519–528, 2012. View at Publisher · View at Google Scholar · View at Scopus
  107. S. Komatsu, D. Ichikawa, H. Takeshita et al., “Circulating miR-18a: a sensitive cancer screening biomarker in human cancer,” In Vivo, vol. 28, no. 3, pp. 293–297, 2014. View at Google Scholar
  108. M. Zhong, Z. Bian, and Z. Wu, “MiR-30a suppresses cell migration and invasion through downregulation of PIK3CD in colorectal carcinoma,” Cellular Physiology and Biochemistry, vol. 31, no. 2-3, pp. 209–218, 2013. View at Publisher · View at Google Scholar · View at Scopus
  109. J. Wu, J. Qian, C. Li et al., “miR-129 regulates cell proliferation by downregulating Cdk6 expression,” Cell Cycle, vol. 9, no. 9, pp. 1809–1818, 2010. View at Publisher · View at Google Scholar · View at Scopus
  110. J. Banzhaf-Strathmann and D. Edbauer, “Good guy or bad guy: the opposing roles of microRNA 125b in cancer,” Cell Communication and Signaling, vol. 12, no. 1, article 30, 2014. View at Publisher · View at Google Scholar · View at Scopus
  111. T. Li, J. Yang, X. Lv et al., “miR-155 regulates the proliferation and cell cycle of colorectal carcinoma cells by targeting E2F2,” Biotechnology Letters, vol. 36, no. 9, pp. 1743–1752, 2014. View at Publisher · View at Google Scholar · View at Scopus
  112. J. Li, Y. Chen, J. Zhao, F. Kong, and Y. Zhang, “MiR-203 reverses chemoresistance in p53-mutated colon cancer cells through downregulation of Akt2 expression,” Cancer Letters, vol. 304, no. 1, pp. 52–59, 2011. View at Publisher · View at Google Scholar · View at Scopus
  113. L. Wu, H. Li, C. Y. Jia et al., “MicroRNA-223 regulates FOXO1 expression and cell proliferation,” FEBS Letters, vol. 586, no. 7, pp. 1038–1043, 2012. View at Publisher · View at Google Scholar · View at Scopus
  114. J. J. Arcaroli, K. S. Quackenbush, R. W. Powell et al., “Common PIK3CA mutants and a novel 3 UTR mutation are associated with increased sensitivity to saracatinib,” Clinical Cancer Research, vol. 18, no. 9, pp. 2704–2714, 2012. View at Publisher · View at Google Scholar · View at Scopus
  115. X. Wang, J. Wang, H. Ma, J. Zhang, and X. Zhou, “Downregulation of miR-195 correlates with lymph node metastasis and poor prognosis in colorectal cancer,” Medical Oncology, vol. 29, no. 2, pp. 919–927, 2012. View at Publisher · View at Google Scholar · View at Scopus
  116. M. L. Chen, L. S. Liang, and X. K. Wang, “MiR-200c inhibits invasion and migration in human colon cancer cells SW480/620 by targeting ZEB1,” Clinical & Experimental Metastasis, vol. 29, no. 5, pp. 457–469, 2012. View at Publisher · View at Google Scholar · View at Scopus
  117. S. Alvarez-Díaz, N. Valle, G. Ferrer-Mayorga et al., “MicroRNA-22 is induced by vitamin D and contributes to its antiproliferative, antimigratory and gene regulatory effects in colon cancer cells,” Human Molecular Genetics, vol. 21, no. 10, pp. 2157–2165, 2012. View at Publisher · View at Google Scholar · View at Scopus
  118. L.-G. Wang and J. Gu, “Serum microRNA-29a is a promising novel marker for early detection of colorectal liver metastasis,” Cancer Epidemiology, vol. 36, no. 1, pp. e61–e67, 2012. View at Publisher · View at Google Scholar · View at Scopus
  119. Y. Zhang, X. He, Y. Liu et al., “MicroRNA-320a inhibits tumor invasion by targeting neuropilin 1 and is associated with liver metastasis in colorectal cancer,” Oncology Reports, vol. 27, no. 3, pp. 685–694, 2012. View at Publisher · View at Google Scholar · View at Scopus
  120. K. Okamoto, T. Ishiguro, Y. Midorikawa et al., “MiR-493 induction during carcinogenesis blocks metastatic settlement of colon cancer cells in liver,” The EMBO Journal, vol. 31, no. 7, pp. 1752–1763, 2012. View at Publisher · View at Google Scholar · View at Scopus
  121. H. Sakai, A. Sato, Y. Aihara et al., “MKK7 mediates miR-493-dependent suppression of liver metastasis of colon cancer cells,” Cancer Science, vol. 105, no. 4, pp. 425–430, 2014. View at Publisher · View at Google Scholar · View at Scopus
  122. X. Liu, Z. Zhang, L. Sun et al., “MicroRNA-499-5p promotes cellular invasion and tumor metastasis in colorectal cancer by targeting FOXO4 and PDCD4,” Carcinogenesis, vol. 32, no. 12, Article ID bgr213, pp. 1798–1805, 2011. View at Publisher · View at Google Scholar · View at Scopus
  123. Z. Cui, J. Tang, J. Chen, and Z. Wang, “Hsa-miR-574-5p negatively regulates MACC-1 expression to suppress colorectal cancer liver metastasis,” Cancer Cell International, vol. 14, article 47, 2014. View at Publisher · View at Google Scholar · View at Scopus