Table of Contents Author Guidelines Submit a Manuscript
Disease Markers
Volume 2017 (2017), Article ID 8245345, 8 pages
https://doi.org/10.1155/2017/8245345
Review Article

MicroRNAs Involvement in Radioresistance of Head and Neck Cancer

1Central European Institute of Technology, Masaryk University, Brno, Czech Republic
2Department of Comprehensive Cancer Care, Masaryk Memorial Cancer Institute, Faculty of Medicine, Masaryk University, Brno, Czech Republic
3Department of Radiation Oncology, Masaryk Memorial Cancer Institute, Brno, Czech Republic
4Department of Otorhinolaryngology and Head and Neck Surgery, St. Anne’s Faculty Hospital, Masaryk University, Brno, Czech Republic

Correspondence should be addressed to Ondrej Slaby

Received 27 December 2016; Accepted 12 February 2017; Published 23 February 2017

Academic Editor: Alvaro González

Copyright © 2017 Parwez Ahmad 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. Janiszewska, M. Szaumkessel, and K. Szyfter, “MicroRNAs are important players in head and neck carcinoma: a review,” Critical Reviews in Oncology/Hematology, vol. 88, no. 3, pp. 716–728, 2013. View at Publisher · View at Google Scholar · View at Scopus
  2. F. Cellini, A. G. Morganti, D. Genovesi, N. Silvestris, and V. Valentini, “Role of microRNA in response to ionizing radiations: evidences and potential impact on clinical practice for radiotherapy,” Molecules, vol. 19, no. 4, pp. 5379–5401, 2014. View at Publisher · View at Google Scholar · View at Scopus
  3. F. Perri, R. Pacelli, G. Della Vittoria Scarpati et al., “Radioresistance in head and neck squamous cell carcinoma: biological bases and therapeutic implications,” Head and Neck, vol. 37, no. 5, pp. 763–770, 2015. View at Publisher · View at Google Scholar · View at Scopus
  4. G. Courthod, P. Franco, L. Palermo, S. Pisconti, and G. Numico, “The role of microRNA in head and neck cancer: current knowledge and perspectives,” Molecules, vol. 19, no. 5, pp. 5704–5716, 2014. View at Publisher · View at Google Scholar · View at Scopus
  5. T. Zhang, Q. Sun, T. Liu et al., “MiR-451 increases radiosensitivity of nasopharyngeal carcinoma cells by targeting ras-related protein 14 (RAB14),” Tumor Biology, vol. 35, no. 12, pp. 12593–12599, 2014. View at Publisher · View at Google Scholar · View at Scopus
  6. N. Lynam-Lennon, J. V. Reynolds, L. Marignol, O. M. Sheils, G. P. Pidgeon, and S. G. Maher, “MicroRNA-31 modulates tumour sensitivity to radiation in oesophageal adenocarcinoma,” Journal of Molecular Medicine, vol. 90, no. 12, pp. 1449–1458, 2012. View at Publisher · View at Google Scholar · View at Scopus
  7. C.-J. Liu, M.-M. Tsai, P.-S. Hung et al., “miR-31 ablates expression of the HIF regulatory factor FIH to activate the HIF pathway in head and neck carcinoma,” Cancer Research, vol. 70, no. 4, pp. 1635–1644, 2010. View at Publisher · View at Google Scholar · View at Scopus
  8. N. Liu, R. J. Boohaker, C. Jiang, J. R. Boohaker, and B. Xu, “A radiosensitivity MiRNA signature validated by the TCGA database for head and neck squamous cell carcinomas,” Oncotarget, vol. 6, no. 33, pp. 34649–34657, 2015. View at Publisher · View at Google Scholar · View at Scopus
  9. Y.-E. Suh, N. Raulf, J. Gäken et al., “MicroRNA-196a promotes an oncogenic effect in head and neck cancer cells by suppressing annexin A1 and enhancing radioresistance,” International Journal of Cancer, vol. 137, no. 5, pp. 1021–1034, 2015. View at Publisher · View at Google Scholar · View at Scopus
  10. H. E. Gee, C. Camps, F. M. Buffa et al., “hsa-mir-210 is a marker of tumor hypoxia and a prognostic factor in head and neck cancer,” Cancer, vol. 116, no. 9, pp. 2148–2158, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. G. Li, Y. Qiu, Z. Su et al., “Genome-wide analyses of radioresistance-associated miRNA expression profile in nasopharyngeal carcinoma using next generation deep sequencing,” PLoS ONE, vol. 8, no. 12, Article ID e84486, 2013. View at Publisher · View at Google Scholar · View at Scopus
  12. C. Qu, Z. Liang, J. Huang et al., “MiR-205 determines the radioresistance of human nasopharyngeal carcinoma by directly targeting PTEN,” Cell Cycle, vol. 11, no. 4, pp. 785–796, 2012. View at Publisher · View at Google Scholar · View at Scopus
  13. X.-H. Li, J.-Q. Qu, H. Yi et al., “Integrated analysis of differential miRNA and mRNA expression profiles in human radioresistant and radiosensitive nasopharyngeal carcinoma cells,” PLoS ONE, vol. 9, no. 1, Article ID e87767, 2014. View at Publisher · View at Google Scholar · View at Scopus
  14. H. Xia, S. Chen, K. Chen, H. Huang, and H. Ma, “MiR-96 promotes proliferation and chemo- or radioresistance by down-regulating RECK in esophageal cancer,” Biomedicine and Pharmacotherapy, vol. 68, no. 8, pp. 951–958, 2014. View at Publisher · View at Google Scholar · View at Scopus
  15. D. Maia, A. C. de Carvalho, M. A. Horst, A. L. Carvalho, C. Scapulatempo-Neto, and A. L. Vettore, “Expression of miR-296-5p as predictive marker for radiotherapy resistance in early-stage laryngeal carcinoma,” Journal of Translational Medicine, vol. 13, article 262, 2015. View at Publisher · View at Google Scholar · View at Scopus
  16. H. Zhu, X. Zhu, G. Cheng, M. Zhou, and W. Lou, “Downregulation of microRNA-21 enhances radiosensitivity in nasopharyngeal carcinoma,” Experimental and Therapeutic Medicine, vol. 9, no. 6, pp. 2185–2189, 2015. View at Publisher · View at Google Scholar · View at Scopus
  17. S. Huang, X.-Q. Li, X. Chen, S.-M. Che, W. Chen, and X.-Z. Zhang, “Inhibition of microRNA-21 increases radiosensitivity of esophageal cancer cells through phosphatase and tensin homolog deleted on chromosome 10 activation,” Diseases of the Esophagus, vol. 26, no. 8, pp. 823–831, 2013. View at Publisher · View at Google Scholar · View at Scopus
  18. H. Su, X. Jin, X. Zhang et al., “Identification of microRNAs involved in the radioresistance of esophageal cancer cells,” Cell Biology International, vol. 38, no. 3, pp. 318–325, 2014. View at Publisher · View at Google Scholar · View at Scopus
  19. L. Xu, Z. Chen, F. Xue et al., “MicroRNA-24 inhibits growth, induces apoptosis, and reverses radioresistance in laryngeal squamous cell carcinoma by targeting X-linked inhibitor of apoptosis protein,” Cancer Cell International, vol. 15, article 61, 2015. View at Publisher · View at Google Scholar · View at Scopus
  20. S. Wang, R. Zhang, F. X. Claret, and H. Yang, “Involvement of microRNA-24 and DNA methylation in resistance of nasopharyngeal carcinoma to ionizing radiation,” Molecular Cancer Therapeutics, vol. 13, no. 12, pp. 3163–3174, 2014. View at Publisher · View at Google Scholar · View at Scopus
  21. G. Li, Y. Liu, Z. Su et al., “MicroRNA-324-3p regulates nasopharyngeal carcinoma radioresistance by directly targeting WNT2B,” European Journal of Cancer, vol. 49, no. 11, pp. 2596–2607, 2013. View at Publisher · View at Google Scholar · View at Scopus
  22. Z. Long, B. Wang, D. Tao, Y. Huang, and Z. Tao, “Hypofractionated radiotherapy induces miR-34a expression and enhances apoptosis in human nasopharyngeal carcinoma cells,” International Journal of Molecular Medicine, vol. 34, no. 5, pp. 1388–1394, 2014. View at Publisher · View at Google Scholar · View at Scopus
  23. G. Li, Y. Wang, Y. Liu et al., “miR-185-3p regulates nasopharyngeal carcinoma radioresistance by targeting WNT2B in vitro,” Cancer Science, vol. 105, no. 12, pp. 1560–1568, 2014. View at Publisher · View at Google Scholar · View at Scopus
  24. S. Zhou, W. Ye, J. Ren et al., “MicroRNA-381 increases radiosensitivity in esophageal squamous cell carcinoma,” American Journal of Cancer Research, vol. 5, pp. 267–277, 2015. View at Google Scholar
  25. M. Shiiba, K. Shinozuka, K. Saito et al., “MicroRNA-125b regulates proliferation and radioresistance of oral squamous cell carcinoma,” British Journal of Cancer, vol. 108, no. 9, pp. 1817–1821, 2013. View at Publisher · View at Google Scholar · View at Scopus
  26. S.-Y. Wu, K.-C. Lin, J.-F. Chiou et al., “MicroRNA-17-5p post-transcriptionally regulates p21 expression in irradiated betel quid chewing-related oral squamous cell carcinoma cells,” Strahlentherapie und Onkologie, vol. 189, no. 8, pp. 675–683, 2013. View at Publisher · View at Google Scholar · View at Scopus
  27. M. C. de Jong, J. J. Ten Hoeve, R. Grénman et al., “Pretreatment microRNA expression impacting on epithelial-to-mesenchymal transition predicts intrinsic radiosensitivity in head and neck cancer cell lines and patients,” Clinical Cancer Research, vol. 21, no. 24, pp. 5630–5638, 2015. View at Publisher · View at Google Scholar · View at Scopus
  28. J.-Q. Qu, H.-M. Yi, X. Ye et al., “MiRNA-203 reduces nasopharyngeal carcinoma radioresistance by targeting IL8/AKT signaling,” Molecular Cancer Therapeutics, vol. 14, no. 11, pp. 2653–2664, 2015. View at Publisher · View at Google Scholar · View at Scopus
  29. C. Metheetrairut and F. J. Slack, “MicroRNAs in the ionizing radiation response and in radiotherapy,” Current Opinion in Genetics and Development, vol. 23, no. 1, pp. 12–19, 2013. View at Publisher · View at Google Scholar · View at Scopus
  30. F. Ganci, A. Sacconi, V. Manciocco et al., “Radioresistance in head and neck squamous cell carcinoma—possible molecular markers for local recurrence and new putative therapeutic strategies,” in Contemporary Issues in Head and Neck Cancer Management, InTech, 2015. View at Google Scholar
  31. E. Korpela, D. Vesprini, and S. K. Liu, “MicroRNA in radiotherapy: miRage or miRador?” British Journal of Cancer, vol. 112, no. 5, pp. 777–782, 2015. View at Publisher · View at Google Scholar · View at Scopus
  32. M. Zimmermann, A. Zouhair, D. Azria, and M. Ozsahin, “The epidermal growth factor receptor (EGFR) in head and neck cancer: its role and treatment implications,” Radiation Oncology, vol. 1, no. 1, article 11, 2006. View at Publisher · View at Google Scholar · View at Scopus
  33. M. Olivier, M. Hollstein, and P. Hainaut, “TP53 mutations in human cancers: origins, consequences, and clinical use,” Cold Spring Harbor Perspectives in Biology, vol. 2, no. 1, Article ID a001008, 2010. View at Publisher · View at Google Scholar · View at Scopus
  34. A. M. Gross, R. K. Orosco, J. P. Shen et al., “Multi-tiered genomic analysis of head and neck cancer ties TP53 mutation to 3p loss,” Nature Genetics, vol. 46, no. 9, pp. 939–943, 2014. View at Publisher · View at Google Scholar · View at Scopus
  35. J. K. Peltonen, K. H. Vähäkangas, H. M. Helppi, R. Bloigu, P. Pääkkö, and T. Turpeenniemi-Hujanen, “Specific TP53 mutations predict aggressive phenotype in head and neck squamous cell carcinoma: a retrospective archival study,” Head and Neck Oncology, vol. 3, no. 1, article 20, 2011. View at Publisher · View at Google Scholar · View at Scopus
  36. M. L. Poeta, J. Manola, M. A. Goldwasser et al., “TP53 mutations and survival in squamous-cell carcinoma of the head and neck,” The New England Journal of Medicine, vol. 357, no. 25, pp. 2552–2561, 2007. View at Publisher · View at Google Scholar · View at Scopus
  37. H. D. Skinner, V. C. Sandulache, T. J. Ow et al., “TP53 disruptive mutations lead to head and neck cancer treatment failure through inhibition of radiation-induced senescence,” Clinical Cancer Research, vol. 18, no. 1, pp. 290–300, 2012. View at Publisher · View at Google Scholar · View at Scopus
  38. S. Patan, “Vasculogenesis and angiogenesis,” Cancer Treatment and Research, vol. 117, pp. 3–32, 2004. View at Publisher · View at Google Scholar · View at Scopus
  39. H. E. Barker, J. T. E. Paget, A. A. Khan, and K. J. Harrington, “The tumour microenvironment after radiotherapy: mechanisms of resistance and recurrence,” Nature Reviews Cancer, vol. 15, no. 7, pp. 409–425, 2015. View at Publisher · View at Google Scholar · View at Scopus
  40. T. W. H. Meijer, J. H. A. M. Kaanders, P. N. Span, and J. Bussink, “Targeting hypoxia, HIF-1, and tumor glucose metabolism to improve radiotherapy efficacy,” Clinical Cancer Research, vol. 18, no. 20, pp. 5585–5594, 2012. View at Publisher · View at Google Scholar · View at Scopus
  41. J. M. Brown, “Vasculogenesis: a crucial player in the resistance of solid tumours to radiotherapy,” The British journal of radiology, vol. 87, no. 1035, 2014. View at Publisher · View at Google Scholar · View at Scopus
  42. M. J. Cross and L. Claesson-Welsh, “FGF and VEGF function in angiogenesis: signalling pathways, biological responses and therapeutic inhibition,” Trends in Pharmacological Sciences, vol. 22, no. 4, pp. 201–207, 2001. View at Publisher · View at Google Scholar · View at Scopus
  43. R. Kalluri and E. G. Neilson, “Epithelial-mesenchymal transition and its implications for fibrosis,” The Journal of Clinical Investigation, vol. 112, no. 12, pp. 1776–1784, 2003. View at Publisher · View at Google Scholar · View at Scopus
  44. R. Kalluri and R. A. Weinberg, “The basics of epithelial-mesenchymal transition,” Journal of Clinical Investigation, vol. 119, no. 6, pp. 1420–1428, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. L. Chang, P. H. Graham, J. Hao et al., “Acquisition of epithelialmesenchymal transition and cancer stem cell phenotypes is associated with activation of the PI3K/Akt/mTOR pathway in prostate cancer radioresistance,” Cell Death and Disease, vol. 4, no. 10, article e875, 2013. View at Publisher · View at Google Scholar · View at Scopus
  46. Y.-C. Zhou, J.-Y. Liu, J. Li et al., “Ionizing radiation promotes migration and invasion of cancer cells through transforming growth factor-beta-mediated epithelial-mesenchymal transition,” International Journal of Radiation Oncology Biology Physics, vol. 81, no. 5, pp. 1530–1537, 2011. View at Publisher · View at Google Scholar · View at Scopus
  47. S. A. Mani, W. Guo, M.-J. Liao et al., “The epithelial-mesenchymal transition generates cells with properties of stem cells,” Cell, vol. 133, no. 4, pp. 704–715, 2008. View at Publisher · View at Google Scholar · View at Scopus
  48. A. Kreso and J. E. Dick, “Evolution of the cancer stem cell model,” Cell Stem Cell, vol. 14, no. 3, pp. 275–291, 2014. View at Publisher · View at Google Scholar · View at Scopus
  49. R. Kleinová, O. Slabý, and J. Šáňa, “The relevance of microRNAs in glioblastoma stem cells,” Klinicka onkologie, vol. 28, no. 5, pp. 338–344, 2015. View at Publisher · View at Google Scholar
  50. S. Krishnamurthy and J. E. Nör, “Head and neck cancer stem cells,” Journal of Dental Research, vol. 91, no. 4, pp. 334–340, 2012. View at Publisher · View at Google Scholar · View at Scopus
  51. J. Han, T. Fujisawa, S. R. Husain, and R. K. Puri, “Identification and characterization of cancer stem cells in human head and neck squamous cell carcinoma,” BMC Cancer, vol. 14, no. 1, article 173, 2014. View at Publisher · View at Google Scholar · View at Scopus
  52. M. I. Koukourakis, A. Giatromanolaki, V. Tsakmaki, V. Danielidis, and E. Sivridis, “Cancer stem cell phenotype relates to radio-chemotherapy outcome in locally advanced squamous cell head-neck cancer,” British Journal of Cancer, vol. 106, no. 5, pp. 846–853, 2012. View at Publisher · View at Google Scholar · View at Scopus
  53. A. Besse, J. Sana, P. Fadrus, and O. Slaby, “MicroRNAs involved in chemo- and radioresistance of high-grade gliomas,” Tumor Biology, vol. 34, no. 4, pp. 1969–1978, 2013. View at Publisher · View at Google Scholar · View at Scopus
  54. L. Zhao, A. M. Bode, Y. Cao, and Z. Dong, “Regulatory mechanisms and clinical perspectives of miRNA in tumor radiosensitivity,” Carcinogenesis, vol. 33, no. 11, pp. 2220–2227, 2012. View at Publisher · View at Google Scholar · View at Scopus
  55. H.-S. Gwak, T. H. Kim, G. H. Jo et al., “Silencing of microRNA-21 confers radio-sensitivity through inhibition of the PI3K/AKT pathway and enhancing autophagy in malignant glioma cell lines,” PLoS ONE, vol. 7, no. 10, Article ID e47449, 2012. View at Publisher · View at Google Scholar · View at Scopus
  56. J. Zhang, C. Zhang, L. Hu et al., “Abnormal expression of miR-21 and miR-95 in cancer stem-like cells is associated with radioresistance of lung cancer,” Cancer Investigation, vol. 33, no. 5, pp. 165–171, 2015. View at Publisher · View at Google Scholar · View at Scopus
  57. S. Liu, L. Song, L. Zhang, S. Zeng, and F. Gao, “MiR-21 modulates resistance of HR-HPV positive cervical cancer cells to radiation through targeting LATS1,” Biochemical and Biophysical Research Communications, vol. 459, no. 4, pp. 679–685, 2015. View at Publisher · View at Google Scholar · View at Scopus
  58. W. Li, F. Guo, P. Wang, S. Hong, and C. Zhang, “miR-221/222 confers radioresistance in glioblastoma cells through activating Akt independent of PTEN status,” Current Molecular Medicine, vol. 14, no. 1, pp. 185–195, 2014. View at Publisher · View at Google Scholar · View at Scopus
  59. Z. Chun-Zhi, H. Lei, Z. An-Ling et al., “MicroRNA-221 and microRNA-222 regulate gastric carcinoma cell proliferation and radioresistance by targeting PTEN,” BMC Cancer, vol. 10, article 367, 2010. View at Publisher · View at Google Scholar · View at Scopus
  60. Y. Zhang, L. Zheng, Y. Ding et al., “MIR-20a Induces Cell Radioresistance by Activating the PTEN/PI3K/Akt Signaling Pathway in Hepatocellular Carcinoma,” International Journal of Radiation Oncology Biology Physics, vol. 92, no. 5, pp. 1132–1140, 2015. View at Publisher · View at Google Scholar · View at Scopus
  61. W. Yang, T. Sun, J. Cao, F. Liu, Y. Tian, and W. Zhu, “Downregulation of miR-210 expression inhibits proliferation, induces apoptosis and enhances radiosensitivity in hypoxic human hepatoma cells in vitro,” Experimental Cell Research, vol. 318, no. 8, pp. 944–954, 2012. View at Publisher · View at Google Scholar · View at Scopus
  62. Y. Sun, X. Xing, Q. Liu et al., “Hypoxia-induced autophagy reduces radiosensitivity by the HIF-1α/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 · View at Scopus
  63. M. E. Crosby, R. Kulshreshtha, M. Ivan, and P. M. Glazer, “MicroRNA regulation of DNA repair gene expression in hypoxic stress,” Cancer Research, vol. 69, no. 3, pp. 1221–1229, 2009. View at Publisher · View at Google Scholar · View at Scopus
  64. Q. Sun, T. Liu, Y. Yuan et al., “MiR-200c inhibits autophagy and enhances radiosensitivity in breast cancer cells by targeting UBQLN1,” International Journal of Cancer, vol. 136, no. 5, pp. 1003–1012, 2015. View at Publisher · View at Google Scholar · View at Scopus
  65. P. Gasparini, F. Lovat, M. Fassan et al., “Protective role of miR-155 in breast cancer through RAD51 targeting impairs homologous recombination after irradiation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 111, no. 12, pp. 4536–4541, 2014. View at Publisher · View at Google Scholar · View at Scopus
  66. P. Zhang, L. Wang, C. Rodriguez-Aguayo et al., “MiR-205 acts as a tumour radiosensitizer by targeting ZEB1 and Ubc13,” Nature Communications, vol. 5, article 5671, 2014. View at Publisher · View at Google Scholar · View at Scopus
  67. L. Ye, G. Yu, C. Wang et al., “MicroRNA-128a, BMI1 polycomb ring finger oncogene, and reactive oxygen species inhibit the growth of U-87 MG glioblastoma cells following exposure to X-ray radiation,” Molecular Medicine Reports, vol. 12, no. 4, pp. 6247–6254, 2015. View at Publisher · View at Google Scholar · View at Scopus
  68. S. Xiao, Z. Yang, R. Lv et al., “miR-135b contributes to the radioresistance by targeting GSK3β in human glioblastoma multiforme cells,” PLoS ONE, vol. 9, no. 9, Article ID e108810, 2014. View at Publisher · View at Google Scholar · View at Scopus
  69. P. Moskwa, P. O. Zinn, Y. E. Choi et al., “A functional screen identifies miRs that induce radioresistance in glioblastomas,” Molecular Cancer Research, vol. 12, no. 12, pp. 1767–1778, 2014. View at Publisher · View at Google Scholar · View at Scopus
  70. A. Besse, J. Sana, R. Lakomy et al., “MiR-338-5p sensitizes glioblastoma cells to radiation through regulation of genes involved in DNA damage response,” Tumor Biology, vol. 37, no. 6, pp. 7719–7727, 2016. View at Publisher · View at Google Scholar · View at Scopus
  71. Y. Li, W. Han, T.-T. Ni et al., “Knockdown of microRNA-1323 restores sensitivity to radiation by suppression of PRKDC activity in radiation-resistant lung cancer cells,” Oncology Reports, vol. 33, no. 6, pp. 2821–2828, 2015. View at Publisher · View at Google Scholar · View at Scopus
  72. H.-H. Zhang, M. Pang, W. Dong et al., “MiR-511 induces the apoptosis of radioresistant lung adenocarcinoma cells by triggering BAX,” Oncology Reports, vol. 31, no. 3, pp. 1473–1479, 2014. View at Publisher · View at Google Scholar · View at Scopus
  73. Z. Shen, X. Wu, Z. Wang, B. Li, and X. Zhu, “Effect of miR-18a overexpression on the radiosensitivity of non-small cell lung cancer,” International Journal of Clinical and Experimental Pathology, vol. 8, no. 1, pp. 643–648, 2015. View at Google Scholar · View at Scopus
  74. X.-D. Yang, X.-H. Xu, S.-Y. Zhang et al., “Role of miR-100 in the radioresistance of colorectal cancer cells,” American Journal of Cancer Research, vol. 5, pp. 545–559, 2015. View at Google Scholar
  75. Y. Zhang, L. Zheng, J. Huang et al., “MiR-124 radiosensitizes human colorectal cancer cells by targeting PRRX1,” PLoS ONE, vol. 9, no. 4, Article ID e93917, 2014. View at Publisher · View at Google Scholar · View at Scopus