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The emerging role of noncoding RNAs in colorectal cancer chemoresistance

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Abstract

Background

Colorectal cancer (CRC) is the third most prevalent cancer in the world and one of the most lethal human malignancies. Chemotherapy with 5-fluorouracil, platinum, hydroxycamptothecin, vincristine, methotrexate, irinotecan, paclitaxel and/or cetuximab has significantly improved the survival of CRC patients. However, most CRC patients eventually develop chemoresistance, resulting in a poor prognosis. The mechanisms involved in CRC chemoresistance are complex and, as yet, inconclusive. Noncoding RNAs (ncRNAs), such as small nucleolar RNAs (snoRNAs), microRNAs (miRNAs) and long noncoding RNAs (lncRNAs), represent transcripts without protein-coding potential. Accumulating evidence indicates that multiple deregulated ncRNAs, including miRNAs and lncRNAs, play pivotal roles in the development of chemoresistance in CRC. This notion has potential clinical implications.

Conclusions

In this review, we highlight the emerging roles and the regulatory mechanisms by which miRNAs and lncRNAs affect CRC chemoresistance. Tumor-specific miRNAs and lncRNAs may serve as novel therapeutic targets and prognostic biomarkers for CRC.

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References

  1. R.L. Siegel, K.D. Miller, A. Jemal, Cancer statistics, 2015. CA Cancer J. Clin. 65, 5–29 (2015)

    PubMed  Google Scholar 

  2. S. Rosello, F. Papaccio, D. Roda, N. Tarazona, A. Cervantes, The role of chemotherapy in localized and locally advanced rectal cancer: A systematic revision. Cancer Treat. Rev. 63, 156–171 (2018)

    CAS  PubMed  Google Scholar 

  3. A.T. Nies, T. Magdy, M. Schwab, U.M. Zanger, Role of ABC transporters in fluoropyrimidine-based chemotherapy response. Adv. Cancer Res. 125, 217–243 (2015)

    CAS  PubMed  Google Scholar 

  4. W.A. Hammond, A. Swaika, K. Mody, Pharmacologic resistance in colorectal cancer: A review. Ther. Adv. Med. Oncol. 8, 57–84 (2016)

    Google Scholar 

  5. P.E. Czabotar, G. Lessene, A. Strasser, J.M. Adams, Control of apoptosis by the BCL-2 protein family: Implications for physiology and therapy. Nat. Rev. Mol. Cell Biol. 15, 49–63 (2014)

    CAS  PubMed  Google Scholar 

  6. S. Djebali, C.A. Davis, A. Merkel, A. Dobin, T. Lassmann, A. Mortazavi, A. Tanzer, J. Lagarde, W. Lin, F. Schlesinger, C. Xue, G.K. Marinov, J. Khatun, B.A. Williams, C. Zaleski, J. Rozowsky, M. Roder, F. Kokocinski, R.F. Abdelhamid, T. Alioto, I. Antoshechkin, M.T. Baer, N.S. Bar, P. Batut, K. Bell, I. Bell, S. Chakrabortty, X. Chen, J. Chrast, J. Curado, T. Derrien, J. Drenkow, E. Dumais, J. Dumais, R. Duttagupta, E. Falconnet, M. Fastuca, K. Fejes-Toth, P. Ferreira, S. Foissac, M.J. Fullwood, H. Gao, D. Gonzalez, A. Gordon, H. Gunawardena, C. Howald, S. Jha, R. Johnson, P. Kapranov, B. King, C. Kingswood, O.J. Luo, E. Park, K. Persaud, J.B. Preall, P. Ribeca, B. Risk, D. Robyr, M. Sammeth, L. Schaffer, L.H. See, A. Shahab, J. Skancke, A.M. Suzuki, H. Takahashi, H. Tilgner, D. Trout, N. Walters, H. Wang, J. Wrobel, Y. Yu, X. Ruan, Y. Hayashizaki, J. Harrow, M. Gerstein, T. Hubbard, A. Reymond, S.E. Antonarakis, G. Hannon, M.C. Giddings, Y. Ruan, B. Wold, P. Carninci, R. Guigo, T.R. Gingeras, Landscape of transcription in human cells. Nature 489, 101–108 (2012)

    CAS  PubMed  PubMed Central  Google Scholar 

  7. S. Yang, Z. Sun, Q. Zhou, W. Wang, G. Wang, J. Song, Z. Li, Z. Zhang, Y. Chang, K. Xia, J. Liu, W. Yuan, MicroRNAs, long noncoding RNAs, and circular RNAs: Potential tumor biomarkers and targets for colorectal cancer. Cancer Manag. Res. 10, 2249–2257 (2018)

    CAS  PubMed  PubMed Central  Google Scholar 

  8. J. Luo, J. Qu, D.K. Wu, Z.L. Lu, Y.S. Sun, Q. Qu, Long non-coding RNAs: A rising biotarget in colorectal cancer. Oncotarget 8, 22187–22202 (2017)

    PubMed  PubMed Central  Google Scholar 

  9. M. Garofalo, C.M. Croce, microRNAs: Master regulators as potential therapeutics in cancer. Annu. Rev. Pharmacol. Toxicol. 51, 25–43 (2011)

    CAS  PubMed  Google Scholar 

  10. W.K. Wu, P.T. Law, C.W. Lee, C.H. Cho, D. Fan, K. Wu, J. Yu, J.J. Sung, MicroRNA in colorectal cancer: From benchtop to bedside. Carcinogenesis 32, 247–253 (2011)

    CAS  PubMed  Google Scholar 

  11. Y. Qin, L. Li, F. Wang, X. Zhou, Y. Liu, Y. Yin, X. Qi, Knockdown of Mir-135b sensitizes colorectal cancer cells to Oxaliplatin-induced apoptosis through increase of FOXO1. Cell. Physiol. Biochem. 48, 1628–1637 (2018)

    CAS  PubMed  Google Scholar 

  12. D.P. Bartel, MicroRNAs: Target recognition and regulatory functions. Cell 136, 215–233 (2009)

    CAS  PubMed  PubMed Central  Google Scholar 

  13. M. Ul Hussain, Micro-RNAs (miRNAs): Genomic organisation, biogenesis and mode of action. Cell Tissue Res. 349, 405–413 (2012)

    PubMed  Google Scholar 

  14. G.S. Markopoulos, E. Roupakia, M. Tokamani, E. Chavdoula, M. Hatziapostolou, C. Polytarchou, K.B. Marcu, A.G. Papavassiliou, R. Sandaltzopoulos, E. Kolettas, A step-by-step microRNA guide to cancer development and metastasis. Cell. Oncol. 40, 303–339 (2017)

    CAS  Google Scholar 

  15. S. Ebrahimi, S.I. Hashemy, MicroRNA-mediated redox regulation modulates therapy resistance in cancer cells: Clinical perspectives. Cell. Oncol. 42, 131–141 (2019)

    CAS  Google Scholar 

  16. D.B. Longley, D.P. Harkin, P.G. Johnston, 5-fluorouracil: Mechanisms of action and clinical strategies. Nat. Rev. Cancer 3, 330–338 (2003)

    CAS  PubMed  Google Scholar 

  17. P.R. Subbarayan, M. Sarkar, G. Nelson, E. Benitez, S. Singhal, B. Ardalan, Chronic exposure of colorectal cancer cells in culture to fluoropyrimidine analogs induces thymidylate synthase and suppresses p53. A molecular explanation for the mechanism of 5-FU resistance. Anticancer Res. 30, 1149–1156 (2010)

    CAS  PubMed  Google Scholar 

  18. N. Zhang, Y. Yin, S.J. Xu, W.S. Chen, 5-fluorouracil: Mechanisms of resistance and reversal strategies. Molecules 13, 1551–1569 (2008)

    CAS  PubMed  PubMed Central  Google Scholar 

  19. S.J. Dong, X.J. Cai, S.J. Li, The clinical significance of MiR-429 as a predictive biomarker in colorectal cancer patients receiving 5-fluorouracil treatment. Med. Sci. Monit. 22, 3352–3361 (2016)

    CAS  PubMed  PubMed Central  Google Scholar 

  20. J. Chen, W. Wang, Y. Zhang, Y. Chen, T. Hu, Predicting distant metastasis and chemoresistance using plasma miRNAs. Med. Oncol. 31, 799 (2014)

    PubMed  Google Scholar 

  21. H. Chai, M. Liu, R. Tian, X. Li, H. Tang, miR-20a targets BNIP2 and contributes chemotherapeutic resistance in colorectal adenocarcinoma SW480 and SW620 cell lines. Acta Biochim. Biophys. Sin. Shanghai 43, 217–225 (2011)

    CAS  PubMed  Google Scholar 

  22. N. Valeri, P. Gasparini, C. Braconi, A. Paone, F. Lovat, M. Fabbri, K.M. Sumani, H. Alder, D. Amadori, T. Patel, G.J. Nuovo, R. Fishel, C.M. Croce, MicroRNA-21 induces resistance to 5-fluorouracil by down-regulating human DNA MutS homolog 2 (hMSH2). Proc. Natl. Acad. Sci. U. S. A. 107, 21098–21103 (2010)

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Y. Yu, S.S. Kanwar, B.B. Patel, P.S. Oh, J. Nautiyal, F.H. Sarkar, A.P. Majumdar, MicroRNA-21 induces stemness by downregulating transforming growth factor beta receptor 2 (TGFbetaR2) in colon cancer cells. Carcinogenesis 33, 68–76 (2012)

    PubMed  Google Scholar 

  24. B. Song, Y. Wang, Y. Xi, K. Kudo, S. Bruheim, G.I. Botchkina, E. Gavin, Y. Wan, A. Formentini, M. Kornmann, O. Fodstad, J. Ju, Mechanism of chemoresistance mediated by miR-140 in human osteosarcoma and colon cancer cells. Oncogene 28, 4065–4074 (2009)

    CAS  PubMed  PubMed Central  Google Scholar 

  25. V. Boni, N. Bitarte, I. Cristobal, R. Zarate, J. Rodriguez, E. Maiello, J. Garcia-Foncillas, E. Bandres, miR-192/miR-215 influence 5-fluorouracil resistance through cell cycle-mediated mechanisms complementary to its post-transcriptional thymidilate synthase regulation. Mol. Cancer Ther. 9, 2265–2275 (2010)

    CAS  PubMed  Google Scholar 

  26. C. Kim, Y. Hong, H. Lee, H. Kang, E.K. Lee, MicroRNA-195 desensitizes HCT116 human colon cancer cells to 5-fluorouracil. Cancer Lett. 412, 264–271 (2018)

    CAS  PubMed  Google Scholar 

  27. J.B. Kjersem, T. Ikdahl, O.C. Lingjaerde, T. Guren, K.M. Tveit, E.H. Kure, Plasma microRNAs predicting clinical outcome in metastatic colorectal cancer patients receiving first-line oxaliplatin-based treatment. Mol. Oncol. 8, 59–67 (2014)

    CAS  PubMed  Google Scholar 

  28. M. Karaayvaz, H. Zhai, J. Ju, miR-129 promotes apoptosis and enhances chemosensitivity to 5-fluorouracil in colorectal cancer. Cell Death Dis. 4, e659 (2013)

    CAS  PubMed  PubMed Central  Google Scholar 

  29. K. Xu, X. Liang, D. Cui, Y. Wu, W. Shi, J. Liu, miR-1915 inhibits Bcl-2 to modulate multidrug resistance by increasing drug-sensitivity in human colorectal carcinoma cells. Mol. Carcinog. 52, 70–78 (2013)

    CAS  PubMed  Google Scholar 

  30. X. Meng, R. Fu, miR-206 regulates 5-FU resistance by targeting Bcl-2 in colon cancer cells. OncoTargets Ther 11, 1757–1765 (2018)

    Google Scholar 

  31. G. van Niekerk, A.M. Engelbrecht, Role of PKM2 in directing the metabolic fate of glucose in cancer: A potential therapeutic target. Cell. Oncol. 41, 343–351 (2018)

    Google Scholar 

  32. J. He, G. Xie, J. Tong, Y. Peng, H. Huang, J. Li, N. Wang, H. Liang, 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. Biochem. Biophys. 70, 1343–1350 (2014)

    CAS  PubMed  Google Scholar 

  33. Y. Akao, S. Noguchi, A. Iio, K. Kojima, T. Takagi, T. Naoe, Dysregulation of microRNA-34a expression causes drug-resistance to 5-FU in human colon cancer DLD-1 cells. Cancer Lett. 300, 197–204 (2011)

    CAS  PubMed  Google Scholar 

  34. X. Li, H. Zhao, X. Zhou, L. Song, Inhibition of lactate dehydrogenase a by microRNA-34a resensitizes colon cancer cells to 5-fluorouracil. Mol. Med. Rep. 11, 577–582 (2015)

    CAS  PubMed  Google Scholar 

  35. P.M. Borralho, B.T. Kren, R.E. Castro, I.B. da Silva, C.J. Steer, C.M. Rodrigues, MicroRNA-143 reduces viability and increases sensitivity to 5-fluorouracil in HCT116 human colorectal cancer cells. FEBS J. 276, 6689–6700 (2009)

    CAS  PubMed  Google Scholar 

  36. Q. Fu, J. Cheng, J. Zhang, Y. Zhang, X. Chen, S. Luo, J. Xie, miR-20b reduces 5-FU resistance by suppressing the ADAM9/EGFR signaling pathway in colon cancer. Oncol. Rep. 37, 123–130 (2017)

    PubMed  Google Scholar 

  37. Adjuvant chemotherapy with oxaliplatin, in combination with fluorouracil plus leucovorin prolongs disease-free survival, but causes more adverse events in people with stage II or III colon cancer Abstracted from: Andre T, Boni C, Mounedji-Boudiaf L, et al. Multicenter international study of oxaliplatin/5-fluorouracil/leucovorin in the adjuvant treatment of colon cancer (MOSAIC) investigators. Oxaliplatin, fluorouracil, and leucovorin as adjuvant treatment for colon cancer. N. Eng. J. Med. 50, 2343–2351, 2014. Cancer Treat. Rev. 30, 711–713 (2004)

  38. Q. Chen, H.W. Xia, X.J. Ge, Y.C. Zhang, Q.L. Tang, F. Bi, Serum miR-19a predicts resistance to FOLFOX chemotherapy in advanced colorectal cancer cases. Asian Pac. J. Cancer Prev. 14, 7421–7426 (2013)

    PubMed  Google Scholar 

  39. T. Matsumura, K. Sugimachi, H. Iinuma, Y. Takahashi, J. Kurashige, G. Sawada, M. Ueda, R. Uchi, H. Ueo, Y. Takano, Y. Shinden, H. Eguchi, H. Yamamoto, Y. Doki, M. Mori, T. Ochiya, K. Mimori, Exosomal microRNA in serum is a novel biomarker of recurrence in human colorectal cancer. Br. J. Cancer 113, 275–281 (2015)

    CAS  PubMed  PubMed Central  Google Scholar 

  40. L. Perez-Carbonell, F.A. Sinicrope, S.R. Alberts, A.L. Oberg, F. Balaguer, A. Castells, C.R. Boland, A. Goel, MiR-320e is a novel prognostic biomarker in colorectal cancer. Br. J. Cancer 113, 83–90 (2015)

    CAS  PubMed  PubMed Central  Google Scholar 

  41. L. Fang, H. Li, L. Wang, J. Hu, T. Jin, J. Wang, B.B. Yang, MicroRNA-17-5p promotes chemotherapeutic drug resistance and tumour metastasis of colorectal cancer by repressing PTEN expression. Oncotarget 5, 2974–2987 (2014)

    PubMed  PubMed Central  Google Scholar 

  42. J. Han, J. Li, K. Tang, H. Zhang, B. Guo, N. Hou, C. Huang, miR-338-3p confers 5-fluorouracil resistance in p53 mutant colon cancer cells by targeting the mammalian target of rapamycin. Exp. Cell Res. 360, 328–336 (2017)

    CAS  PubMed  Google Scholar 

  43. Y. Zhang, G. Talmon, J. Wang, MicroRNA-587 antagonizes 5-FU-induced apoptosis and confers drug resistance by regulating PPP2R1B expression in colorectal cancer. Cell Death Dis. 6, e1845 (2015)

    CAS  PubMed  PubMed Central  Google Scholar 

  44. N. Liu, J. Li, Z. Zhao, J. Han, T. Jiang, Y. Chen, N. Hou, C. Huang, MicroRNA-302a enhances 5-fluorouracil-induced cell death in human colon cancer cells. Oncol. Rep. 37, 631–639 (2017)

    PubMed  Google Scholar 

  45. J. Chai, W. Dong, C. Xie, L. Wang, D.L. Han, S. Wang, H.L. Guo, Z.L. Zhang, MicroRNA-494 sensitizes colon cancer cells to fluorouracil through regulation of DPYD. IUBMB Life 67, 191–201 (2015)

    CAS  PubMed  Google Scholar 

  46. L.Y. Wan, J. Deng, X.J. Xiang, L. Zhang, F. Yu, J. Chen, Z. Sun, M. Feng, J.P. Xiong, miR-320 enhances the sensitivity of human colon cancer cells to chemoradiotherapy in vitro by targeting FOXM1. Biochem. Biophys. Res. Commun. 457, 125–132 (2015)

    CAS  PubMed  Google Scholar 

  47. M. Takahashi, M. Cuatrecasas, F. Balaguer, K. Hur, Y. Toiyama, A. Castells, C.R. Boland, A. Goel, The clinical significance of MiR-148a as a predictive biomarker in patients with advanced colorectal cancer. PLoS One 7, e46684 (2012)

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Y. Hibino, N. Sakamoto, Y. Naito, K. Goto, H.Z. Oo, K. Sentani, T. Hinoi, H. Ohdan, N. Oue, W. Yasui, Significance of miR-148a in colorectal neoplasia: Downregulation of miR-148a contributes to the carcinogenesis and cell invasion of colorectal Cancer. Pathobiology 82, 233–241 (2015)

    CAS  PubMed  Google Scholar 

  49. C. Liu, C. Eng, J. Shen, Y. Lu, Y. Takata, A. Mehdizadeh, G.J. Chang, M.A. Rodriguez-Bigas, Y. Li, P. Chang, Y. Mao, M.M. Hassan, F. Wang, D. Li, Serum exosomal miR-4772-3p is a predictor of tumor recurrence in stage II and III colon cancer. Oncotarget 7, 76250–76260 (2016)

    PubMed  PubMed Central  Google Scholar 

  50. S.R. Alberts, W.L. Horvath, W.C. Sternfeld, R.M. Goldberg, M.R. Mahoney, S.R. Dakhil, R. Levitt, K. Rowland, S. Nair, D.J. Sargent, J.H. Donohue, Oxaliplatin, fluorouracil, and leucovorin for patients with unresectable liver-only metastases from colorectal cancer: A north central cancer treatment group phase II study. J. Clin. Oncol. 23, 9243–9249 (2005)

    CAS  PubMed  Google Scholar 

  51. L. Zhang, K. Pickard, V. Jenei, M.D. Bullock, A. Bruce, R. Mitter, G. Kelly, C. Paraskeva, J. Strefford, J. Primrose, G.J. Thomas, G. Packham, A.H. Mirnezami, miR-153 supports colorectal cancer progression via pleiotropic effects that enhance invasion and chemotherapeutic resistance. Cancer Res. 73, 6435–6447 (2013)

    CAS  PubMed  Google Scholar 

  52. T. Jiang, L. Ye, Z. Han, Y. Liu, Y. Yang, Z. Peng, J. Fan, miR-19b-3p promotes colon cancer proliferation and oxaliplatin-based chemoresistance by targeting SMAD4: validation by bioinformatics and experimental analyses. J. Exp. Clin. Cancer Res. 36, 131 (2017)

    PubMed  PubMed Central  Google Scholar 

  53. Y. Zhou, G. Wan, R. Spizzo, C. Ivan, R. Mathur, X. Hu, X. Ye, J. Lu, F. Fan, L. Xia, G.A. Calin, L.M. Ellis, X. Lu, miR-203 induces oxaliplatin resistance in colorectal cancer cells by negatively regulating ATM kinase. Mol. Oncol. 8, 83–92 (2014)

    CAS  PubMed  Google Scholar 

  54. M.H. Rasmussen, N.F. Jensen, L.S. Tarpgaard, C. Qvortrup, M.U. Romer, J. Stenvang, T.P. Hansen, L.L. Christensen, J. Lindebjerg, F. Hansen, B.V. Jensen, T.F. Hansen, P. Pfeiffer, N. Brunner, T.F. Orntoft, C.L. Andersen, High expression of microRNA-625-3p is associated with poor response to first-line oxaliplatin based treatment of metastatic colorectal cancer. Mol. Oncol. 7, 637–646 (2013)

    CAS  PubMed  PubMed Central  Google Scholar 

  55. H. Zhou, C. Lin, Y. Zhang, X. Zhang, C. Zhang, P. Zhang, X. Xie and Z. Ren, miR-506 enhances the sensitivity of human colorectal cancer cells to oxaliplatin by suppressing MDR1/P-gp expression. Cell. Prolif. 50 (2017)  https://doi.org/10.1111/cpr.12341

    PubMed Central  Google Scholar 

  56. Y. Guo, Y. Pang, X. Gao, M. Zhao, X. Zhang, H. Zhang, B. Xuan, Y. Wang, MicroRNA-137 chemosensitizes colon cancer cells to the chemotherapeutic drug oxaliplatin (OXA) by targeting YBX1. Cancer Biomark. 18, 1–9 (2017)

    CAS  PubMed  Google Scholar 

  57. S. Tan, H. Shi, M. Ba, S. Lin, H. Tang, X. Zeng, X. Zhang, miR-409-3p sensitizes colon cancer cells to oxaliplatin by inhibiting Beclin-1-mediated autophagy. Int. J. Mol. Med. 37, 1030–1038 (2016)

    CAS  PubMed  Google Scholar 

  58. L. Peng, H. Zhu, J. Wang, H. Sui, H. Zhang, C. Jin, L. Li, T. Xu, R. Miao, MiR-492 is functionally involved in Oxaliplatin resistance in colon cancer cells LS174T via its regulating the expression of CD147. Mol. Cell. Biochem. 405, 73–79 (2015)

    CAS  PubMed  Google Scholar 

  59. K. Xu, X. Liang, K. Shen, L. Sun, D. Cui, Y. Zhao, J. Tian, L. Ni, J. Liu, MiR-222 modulates multidrug resistance in human colorectal carcinoma by down-regulating ADAM-17. Exp. Cell Res. 318, 2168–2177 (2012)

    CAS  PubMed  Google Scholar 

  60. W.H. Dong, Q. Li, X.Y. Zhang, Q. Guo, H. Li, T.Y. Wang, Deep sequencing identifies deregulation of microRNAs involved with vincristine drug-resistance of colon cancer cells. Int. J. Clin. Exp. Pathol. 8, 11524–11530 (2015)

    CAS  PubMed  PubMed Central  Google Scholar 

  61. N. Mencia, E. Selga, V. Noe, C.J. Ciudad, Underexpression of miR-224 in methotrexate resistant human colon cancer cells. Biochem. Pharmacol. 82, 1572–1582 (2011)

    CAS  PubMed  Google Scholar 

  62. J.L. Tong, C.P. Zhang, F. Nie, X.T. Xu, M.M. Zhu, S.D. Xiao, Z.H. Ran, MicroRNA 506 regulates expression of PPAR alpha in hydroxycamptothecin-resistant human colon cancer cells. FEBS Lett. 585, 3560–3568 (2011)

    CAS  PubMed  Google Scholar 

  63. N. Bitarte, E. Bandres, V. Boni, R. Zarate, J. Rodriguez, M. Gonzalez-Huarriz, I. Lopez, J. Javier Sola, M.M. Alonso, P. Fortes, J. Garcia-Foncillas, MicroRNA-451 is involved in the self-renewal, tumorigenicity, and chemoresistance of colorectal cancer stem cells. Stem Cells 29, 1661–1671 (2011)

    CAS  PubMed  Google Scholar 

  64. J. Qu, L. Zhao, P. Zhang, J. Wang, N. Xu, W. Mi, X. Jiang, C. Zhang, J. Qu, MicroRNA-195 chemosensitizes colon cancer cells to the chemotherapeutic drug doxorubicin by targeting the first binding site of BCL2L2 mRNA. J. Cell. Physiol. 230, 535–545 (2015)

    CAS  PubMed  Google Scholar 

  65. G. Yang, O. Jiang, D. Ling, X. Jiang, P. Yuan, G. Zeng, J. Zhu, J. Tian, Y. Weng, D. Wu, MicroRNA-522 reverses drug resistance of doxorubicin-induced HT29 colon cancer cell by targeting ABCB5. Mol. Med. Rep. 12, 3930–3936 (2015)

    CAS  PubMed  Google Scholar 

  66. M.B. Chen, L. Yang, P.H. Lu, X.L. Fu, Y. Zhang, Y.Q. Zhu, Y. Tian, MicroRNA-101 down-regulates sphingosine kinase 1 in colorectal cancer cells. Biochem. Biophys. Res. Commun. 463, 954–960 (2015)

    CAS  PubMed  Google Scholar 

  67. Y. Liu, S. Gao, X. Chen, M. Liu, C. Mao, X. Fang, Overexpression of miR-203 sensitizes paclitaxel (Taxol)-resistant colorectal cancer cells through targeting the salt-inducible kinase 2 (SIK2). Tumor Biol. 37, 12231–12239 (2016)

    CAS  Google Scholar 

  68. J. Li, Y. Zhang, J. Zhao, F. Kong, Y. Chen, Overexpression of miR-22 reverses paclitaxel-induced chemoresistance through activation of PTEN signaling in p53-mutated colon cancer cells. Mol. Cell. Biochem. 357, 31–38 (2011)

    CAS  PubMed  Google Scholar 

  69. P. Mussnich, R. Rosa, R. Bianco, A. Fusco, D. D'Angelo, MiR-199a-5p and miR-375 affect colon cancer cell sensitivity to cetuximab by targeting PHLPP1. Expert Opin. Ther. Targets 19, 1017–1026 (2015)

    CAS  PubMed  Google Scholar 

  70. D. Han, M. Wang, N. Ma, Y. Xu, Y. Jiang, X. Gao, Long noncoding RNAs: Novel players in colorectal cancer. Cancer Lett. 361, 13–21 (2015)

    CAS  PubMed  Google Scholar 

  71. X. Hu, A.K. Sood, C.V. Dang, L. Zhang, The role of long noncoding RNAs in cancer: The dark matter matters. Curr. Opin. Genet. Dev. 48, 8–15 (2018)

    CAS  PubMed  Google Scholar 

  72. M.L. Pecero, J. Salvador-Bofill, S. Molina-Pinelo, Long non-coding RNAs as monitoring tools and therapeutic targets in breast cancer. Cell. Oncol. 42, 1–12 (2019)

    CAS  Google Scholar 

  73. R. Castro-Oropeza, J. Melendez-Zajgla, V. Maldonado, K. Vazquez-Santillan, The emerging role of lncRNAs in the regulation of cancer stem cells. Cell. Oncol. 41, 585–603 (2018)

    Google Scholar 

  74. N. Chen, D. Guo, Q. Xu, M. Yang, D. Wang, M. Peng, Y. Ding, S. Wang, J. Zhou, Long non-coding RNA FEZF1-AS1 facilitates cell proliferation and migration in colorectal carcinoma. Oncotarget 7, 11271–11283 (2016)

    PubMed  PubMed Central  Google Scholar 

  75. Z. Zhang, C. Zhou, Y. Chang, Z. Zhang, Y. Hu, F. Zhang, Y. Lu, L. Zheng, W. Zhang, X. Li, X. Li, Long non-coding RNA CASC11 interacts with hnRNP-K and activates the WNT/beta-catenin pathway to promote growth and metastasis in colorectal cancer. Cancer Lett. 376, 62–73 (2016)

    CAS  PubMed  Google Scholar 

  76. Y. Rui, M. Hu, P. Wang, C. Zhang, H. Xu, Y. Li, Y. Zhang, J. Gu, Q. Wang, LncRNA HOTTIP mediated DKK1 downregulation confers metastasis and invasion in colorectal cancer cells. Histol. Histopathol. 6, 619–630 (2019)

    Google Scholar 

  77. J. Yu, Z. Han, Z. Sun, Y. Wang, M. Zheng, C. Song, LncRNA SLCO4A1-AS1 facilitates growth and metastasis of colorectal cancer through beta-catenin-dependent Wnt pathway. J. Exp. Clin. Cancer Res. 37, 222 (2018)

    PubMed  PubMed Central  Google Scholar 

  78. M. Zhang, W. Weng, Q. Zhang, Y. Wu, S. Ni, C. Tan, M. Xu, H. Sun, C. Liu, P. Wei, X. Du, The lncRNA NEAT1 activates Wnt/beta-catenin signaling and promotes colorectal cancer progression via interacting with DDX5. J. Hematol. Oncol. 11, 113 (2018)

    PubMed  PubMed Central  Google Scholar 

  79. J. Zhou, J. Lin, H. Zhang, F. Zhu, R. Xie, LncRNA HAND2-AS1 sponging miR-1275 suppresses colorectal cancer progression by upregulating KLF14. Biochem. Biophys. Res. Commun. 503, 1848–1853 (2018)

    CAS  PubMed  Google Scholar 

  80. X. Wang, H. Yu, W. Sun, J. Kong, L. Zhang, J. Tang, J. Wang, E. Xu, M. Lai, H. Zhang, The long non-coding RNA CYTOR drives colorectal cancer progression by interacting with NCL and Sam68. Mol. Cancer 17, 110 (2018)

    PubMed  PubMed Central  Google Scholar 

  81. Y. Cai, P. Yan, G. Zhang, W. Yang, H. Wang, X. Cheng, Long non-coding RNA TP73-AS1 sponges miR-194 to promote colorectal cancer cell proliferation, migration and invasion via up-regulating TGFalpha. Cancer Biomark. 23, 145–156 (2018)

    CAS  PubMed  Google Scholar 

  82. X. Yu, Z. Yuan, Z. Yang, D. Chen, T. Kim, Y. Cui, Q. Luo, Z. Liu, Z. Yang, X. Fan, D. Chen, L. Wang, The novel long noncoding RNA u50535 promotes colorectal cancer growth and metastasis by regulating CCL20. Cell Death Dis. 9, 751 (2018)

    PubMed  PubMed Central  Google Scholar 

  83. Y. Ma, Y. Yang, F. Wang, M.P. Moyer, Q. Wei, P. Zhang, Z. Yang, W. Liu, H. Zhang, N. Chen, H. Wang, H. Wang, H. Qin, Long non-coding RNA CCAL regulates colorectal cancer progression by activating Wnt/beta-catenin signalling pathway via suppression of activator protein 2alpha. Gut 65, 1494–1504 (2016)

    CAS  PubMed  Google Scholar 

  84. Y. Wang, D. Zhang, K. Wu, Q. Zhao, Y. Nie, D. Fan, Long noncoding RNA MRUL promotes ABCB1 expression in multidrug-resistant gastric cancer cell sublines. Mol. Cell. Biol. 34, 3182–3193 (2014)

    PubMed  PubMed Central  Google Scholar 

  85. A.R. Ozes, D.F. Miller, O.N. Ozes, F. Fang, Y. Liu, D. Matei, T. Huang, K.P. Nephew, NF-kappaB-HOTAIR axis links DNA damage response, chemoresistance and cellular senescence in ovarian cancer. Oncogene 35, 5350–5361 (2016)

    CAS  PubMed  PubMed Central  Google Scholar 

  86. Z. Liu, M. Sun, K. Lu, J. Liu, M. Zhang, W. Wu, W. De, Z. Wang, R. Wang, The long noncoding RNA HOTAIR contributes to cisplatin resistance of human lung adenocarcinoma cells via downregualtion of p21(WAF1/CIP1) expression. PLoS One 8, e77293 (2013)

    CAS  PubMed  PubMed Central  Google Scholar 

  87. J. Liu, L. Wan, K. Lu, M. Sun, X. Pan, P. Zhang, B. Lu, G. Liu, Z. Wang, The long noncoding RNA MEG3 contributes to cisplatin resistance of human lung adenocarcinoma. PLoS One 10, e0114586 (2015)

    PubMed  PubMed Central  Google Scholar 

  88. Y. Fan, B. Shen, M. Tan, X. Mu, Y. Qin, F. Zhang, Y. Liu, Long non-coding RNA UCA1 increases chemoresistance of bladder cancer cells by regulating Wnt signaling. FEBS J. 281, 1750–1758 (2014)

    CAS  PubMed  Google Scholar 

  89. Y. Han, J. Ye, D. Wu, P. Wu, Z. Chen, J. Chen, S. Gao, J. Huang, LEIGC long non-coding RNA acts as a tumor suppressor in gastric carcinoma by inhibiting the epithelial-to-mesenchymal transition. BMC Cancer 14, 932 (2014)

    PubMed  PubMed Central  Google Scholar 

  90. T. Gutschner, M. Hammerle, M. Eissmann, J. Hsu, Y. Kim, G. Hung, A. Revenko, G. Arun, M. Stentrup, M. Gross, M. Zornig, A.R. MacLeod, D.L. Spector, S. Diederichs, The noncoding RNA MALAT1 is a critical regulator of the metastasis phenotype of lung cancer cells. Cancer Res. 73, 1180–1189 (2013)

    CAS  PubMed  Google Scholar 

  91. Z. Wang, D. Katsaros, N. Biglia, Y. Shen, Y. Fu, L.W.M. Loo, W. Jia, Y. Obata, H. Yu, High expression of long non-coding RNA MALAT1 in breast cancer is associated with poor relapse-free survival. Breast Cancer Res. Treat. 171, 261–271 (2018)

    CAS  PubMed  PubMed Central  Google Scholar 

  92. P. Yuan, W. Cao, Q. Zang, G. Li, X. Guo, J. Fan, The HIF-2alpha-MALAT1-miR-216b axis regulates multi-drug resistance of hepatocellular carcinoma cells via modulating autophagy. Biochem. Biophys. Res. Commun. 478, 1067–1073 (2016)

    CAS  PubMed  Google Scholar 

  93. F. Jiao, H. Hu, T. Han, C. Yuan, L. Wang, Z. Jin, Z. Guo, L. Wang, Long noncoding RNA MALAT-1 enhances stem cell-like phenotypes in pancreatic cancer cells. Int. J. Mol. Sci. 16, 6677–6693 (2015)

    CAS  PubMed  PubMed Central  Google Scholar 

  94. P. Li, X. Zhang, H. Wang, L. Wang, T. Liu, L. Du, Y. Yang, C. Wang, MALAT1 is associated with poor response to Oxaliplatin-based chemotherapy in colorectal cancer patients and promotes chemoresistance through EZH2. Mol. Cancer Ther. 16, 739–751 (2017)

    CAS  PubMed  Google Scholar 

  95. J. Yan, Y. Dang, S. Liu, Y. Zhang, G. Zhang, LncRNA HOTAIR promotes cisplatin resistance in gastric cancer by targeting miR-126 to activate the PI3K/AKT/MRP1 genes. Tumor Biol. 37, 16345–16355 (2016)

    CAS  Google Scholar 

  96. P. Li, X. Zhang, L. Wang, L. Du, Y. Yang, T. Liu, C. Li, C. Wang, lncRNA HOTAIR contributes to 5FU resistance through suppressing miR-218 and activating NF-kappaB/TS signaling in colorectal cancer. Mol. Ther. Nucleic. Acids 8, 356–369 (2017)

    CAS  PubMed  PubMed Central  Google Scholar 

  97. Z. Xiao, Z. Qu, Z. Chen, Z. Fang, K. Zhou, Z. Huang, X. Guo, Y. Zhang, LncRNA HOTAIR is a prognostic biomarker for the proliferation and chemoresistance of colorectal cancer via MiR-203a-3p-mediated Wnt/ss-catenin signaling pathway. Cell. Physiol. Biochem. 46, 1275–1285 (2018)

    CAS  PubMed  Google Scholar 

  98. L. Wang, X. Zhang, L. Sheng, C. Qiu, R. Luo, LINC00473 promotes the Taxol resistance via miR-15a in colorectal cancer. Biosci. Rep. 38 (2018)

  99. Y. Xiao, U.A. Yurievich, S.V. Yosypovych, Long noncoding RNA XIST is a prognostic factor in colorectal cancer and inhibits 5-fluorouracil-induced cell cytotoxicity through promoting thymidylate synthase expression. Oncotarget 8, 83171–83182 (2017)

    PubMed  PubMed Central  Google Scholar 

  100. L. Qiao, X. Liu, Y. Tang, Z. Zhao, J. Zhang, H. Liu, Knockdown of long non-coding RNA prostate cancer-associated ncRNA transcript 1 inhibits multidrug resistance and c-Myc-dependent aggressiveness in colorectal cancer Caco-2 and HT-29 cells. Mol. Cell. Biochem. 441, 99–108 (2018)

    CAS  PubMed  Google Scholar 

  101. Z. Bian, L. Jin, J. Zhang, Y. Yin, C. Quan, Y. Hu, Y. Feng, H. Liu, B. Fei, Y. Mao, L. Zhou, X. Qi, S. Huang, D. Hua, C. Xing, Z. Huang, LncRNA-UCA1 enhances cell proliferation and 5-fluorouracil resistance in colorectal cancer by inhibiting miR-204-5p. Sci. Rep. 6, 23892 (2016)

    CAS  PubMed  PubMed Central  Google Scholar 

  102. P. Han, J.W. Li, B.M. Zhang, J.C. Lv, Y.M. Li, X.Y. Gu, Z.W. Yu, Y.H. Jia, X.F. Bai, L. Li, Y.L. Liu, B.B. Cui, The lncRNA CRNDE promotes colorectal cancer cell proliferation and chemoresistance via miR-181a-5p-mediated regulation of Wnt/beta-catenin signaling. Mol. Cancer 16, 9 (2017)

    PubMed  PubMed Central  Google Scholar 

  103. H. Gao, X. Song, T. Kang, B. Yan, L. Feng, L. Gao, L. Ai, X. Liu, J. Yu, H. Li, Long noncoding RNA CRNDE functions as a competing endogenous RNA to promote metastasis and oxaliplatin resistance by sponging miR-136 in colorectal cancer. Onco Targets Ther. 10, 205–216 (2017)

  104. C. Li, Y. Gao, Y. Li, D. Ding, TUG1 mediates methotrexate resistance in colorectal cancer via miR-186/CPEB2 axis. Biochem. Biophys. Res. Commun. 491, 552–557 (2017)

    CAS  PubMed  Google Scholar 

  105. Z.K. Wang, L. Yang, L.L. Wu, H. Mao, Y.H. Zhou, P.F. Zhang, G.H. Dai, Long non-coding RNA LINC00261 sensitizes human colon cancer cells to cisplatin therapy. Braz. J. Med. Biol. Res. 51, e6793 (2017)

    CAS  PubMed  PubMed Central  Google Scholar 

  106. G. Ping, W. Xiong, L. Zhang, Y. Li, Y. Zhang, Y. Zhao, Silencing long noncoding RNA PVT1 inhibits tumorigenesis and cisplatin resistance of colorectal cancer. Am. J. Transl. Res. 10, 138–149 (2018)

    CAS  PubMed  PubMed Central  Google Scholar 

  107. H. Fan, J.H. Zhu, X.Q. Yao, Knockdown of long noncoding RNA PVT1 reverses multidrug resistance in colorectal cancer cells. Mol. Med. Rep. 17, 8309–8315 (2018)

    CAS  PubMed  PubMed Central  Google Scholar 

  108. B. Yue, D. Cai, C. Liu, C. Fang, D. Yan, Linc00152 functions as a competing endogenous RNA to confer Oxaliplatin resistance and holds prognostic values in Colon Cancer. Mol. Ther. 24, 2064–2077 (2016)

    CAS  PubMed  PubMed Central  Google Scholar 

  109. K. Kang, Y.H. Huang, H.P. Li, S.M. Guo, Expression of UCA1 and MALAT1 long-chain non-coding RNAs in esophageal squamous cell carcinoma tissues is predictive of patient prognosis. Arch. Med. Sci. 14, 752–759 (2018)

    PubMed  PubMed Central  Google Scholar 

  110. K.F. Wu, W.C. Liang, L. Feng, J.X. Pang, M.M. Waye, J.F. Zhang, W.M. Fu, H19 mediates methotrexate resistance in colorectal cancer through activating Wnt/beta-catenin pathway. Exp. Cell Res. 350, 312–317 (2017)

    CAS  PubMed  Google Scholar 

  111. H. Lee, C. Kim, J.L. Ku, W. Kim, S.K. Yoon, H.J. Kuh, J.H. Lee, S.W. Nam, E.K. Lee, A long non-coding RNA snaR contributes to 5-fluorouracil resistance in human colon cancer cells. Mol. Cell 37, 540–546 (2014)

    Google Scholar 

  112. Y. Li, S. Huang, Y. Li, W. Zhang, K. He, M. Zhao, H. Lin, D. Li, H. Zhang, Z. Zheng, C. Huang, Decreased expression of LncRNA SLC25A25-AS1 promotes proliferation, chemoresistance, and EMT in colorectal cancer cells. Tumor Biol. 37, 14205–14215 (2016)

    CAS  Google Scholar 

  113. J. Li, X. Li, C. Cen, X. Ai, C. Lin, G. Hu, The long non-coding RNA ENST00000547547 reduces 5-fluorouracil resistance of colorectal cancer cells via competitive binding to microRNA-31. Oncol. Rep. 39, 217–226 (2018)

    PubMed  Google Scholar 

  114. L. Li, J. Shang, Y. Zhang, S. Liu, Y. Peng, Z. Zhou, H. Pan, X. Wang, L. Chen, Q. Zhao, MEG3 is a prognostic factor for CRC and promotes chemosensitivity by enhancing oxaliplatin-induced cell apoptosis. Oncol. Rep. 38, 1383–1392 (2017)

    CAS  PubMed  PubMed Central  Google Scholar 

  115. H. Wang, H. Li, L. Zhang, D. Yang, Overexpression of MEG3 sensitizes colorectal cancer cells to oxaliplatin through regulation of miR-141/PDCD4 axis. Biomed. Pharmacother. 106, 1607–1615 (2018)

    CAS  PubMed  Google Scholar 

  116. Q.L. Sun, C.P. Zhao, T.Y. Wang, X.B. Hao, X.Y. Wang, X. Zhang, Y.C. Li, Expression profile analysis of long non-coding RNA associated with vincristine resistance in colon cancer cells by next-generation sequencing. Gene 572, 79–86 (2015)

    CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Shandong Provincial Key Laboratory of Radiation Oncology, Cancer Research Center, Shandong Cancer Hospital and Institute, Shandong First Medical University and Shandong Academy of Medical Sciences, Jinan, 250117, Shandong Province, China

    Ling Wei, Xingwu Wang, Liyan Lv, Yan Zheng & Ming Yang

  2. Department of Radiation Oncology, Shandong Cancer Hospital and Institute, Shandong First Medical University and Shandong Academy of Medical Sciences, Jinan, Shandong Province, China

    Nasha Zhang

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  1. Ling Wei
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  2. Xingwu Wang
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  3. Liyan Lv
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  4. Yan Zheng
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  5. Nasha Zhang
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  6. Ming Yang
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Correspondence to Nasha Zhang or Ming Yang.

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This study was financially supported by the National Natural Science Foundation of China (31671300, 31871306), the Taishan Scholars Program of Shandong Province (tsqn20161060), the Science and Technology Development Project of Shandong Province (2016GSF201211) and the Shandong Health Department (2015WS0155).

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Wei, L., Wang, X., Lv, L. et al. The emerging role of noncoding RNAs in colorectal cancer chemoresistance. Cell Oncol. 42, 757–768 (2019). https://doi.org/10.1007/s13402-019-00466-8

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