Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2013, Article ID 407052, 15 pages
http://dx.doi.org/10.1155/2013/407052
Review Article

Deregulation of the miRNAs Expression in Cervical Cancer: Human Papillomavirus Implications

1Instituto de Fisiología Celular (IFC), Universidad Nacional Autónoma de México (UNAM), 04510 México, DF, Mexico
2Departamento de Genética y Biología Molecular, Centro de Investigación y de Estudios, Avanzados, 07360 México, DF, Mexico

Received 30 April 2013; Accepted 17 September 2013

Academic Editor: Fernando Schmitt

Copyright © 2013 Yazmín Gómez-Gómez 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. G. A. Calin and C. M. Croce, “MicroRNA signatures in human cancers,” Nature Reviews Cancer, vol. 6, no. 11, pp. 857–866, 2006. View at Publisher · View at Google Scholar · View at Scopus
  2. B. Zhang, X. Pan, G. P. Cobb, and T. A. Anderson, “MicroRNAs as oncogenes and tumor suppressors,” Developmental Biology, vol. 302, no. 1, pp. 1–12, 2007. View at Publisher · View at Google Scholar · View at Scopus
  3. G. A. Calin and C. M. Croce, “MicroRNA signatures in human cancers,” Nature Reviews Cancer, vol. 6, no. 11, pp. 857–866, 2006. View at Publisher · View at Google Scholar · View at Scopus
  4. O. A. Kent and J. T. Mendell, “A small piece in the cancer puzzle: microRNAs as tumor suppressors and oncogenes,” Oncogene, vol. 25, no. 46, pp. 6188–6196, 2006. View at Publisher · View at Google Scholar · View at Scopus
  5. E. A. Miska, “How microRNAs control cell division, differentiation and death,” Current Opinion in Genetics and Development, vol. 15, no. 5, pp. 563–568, 2005. View at Publisher · View at Google Scholar · View at Scopus
  6. T. A. Farazi, J. I. Spitzer, P. Morozov, and T. Tuschl, “MiRNAs in human cancer,” Journal of Pathology, vol. 223, no. 2, pp. 102–115, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. L. Zhang, J. Huang, N. Yang et al., “MicroRNAs exhibit high frequency genomic alterations in human cancer,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 24, pp. 9136–9141, 2006. View at Publisher · View at Google Scholar · View at Scopus
  8. G. A. Calin, C. Sevignani, C. D. Dumitru et al., “Human microRNA genes are frequently located at fragile sites and genomic regions involved in cancers,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 9, pp. 2999–3004, 2004. View at Publisher · View at Google Scholar · View at Scopus
  9. G. A. Calin, C. D. Dumitru, M. Shimizu et al., “Frequent deletions and down-regulation of micro-RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 24, pp. 15524–15529, 2002. View at Publisher · View at Google Scholar · View at Scopus
  10. S. M. Wilting, P. J. F. Snijders, W. Verlaat et al., “Altered microRNA expression associated with chromosomal changes contributes to cervical carcinogenesis,” Oncogene, 2012. View at Publisher · View at Google Scholar · View at Scopus
  11. X. Wang, S. Tang, S. Y. Le et al., “Aberrant expression of oncogenic and tumor-suppressive microRNAs in cervical cancer is required for cancer cell growth,” PLoS One, vol. 3, no. 7, Article ID e2557, 2008. View at Publisher · View at Google Scholar · View at Scopus
  12. X. Cai, G. Li, L. A. Laimins, and B. R. Cullen, “Human papillomavirus genotype 31 does not express detectable microRNA levels during latent or productive virus replication,” Journal of Virology, vol. 80, no. 21, pp. 10890–10893, 2006. View at Publisher · View at Google Scholar · View at Scopus
  13. L. He, J. M. Thomson, M. T. Hemann et al., “A microRNA polycistron as a potential human oncogene,” Nature, vol. 435, no. 7043, pp. 828–833, 2005. View at Publisher · View at Google Scholar · View at Scopus
  14. L. He, X. He, L. P. Lim et al., “A microRNA component of the p53 tumour suppressor network,” Nature, vol. 447, no. 7148, pp. 1130–1134, 2007. View at Publisher · View at Google Scholar · View at Scopus
  15. C. M. Croce, “Oncogenes and cancer,” The New England Journal of Medicine, vol. 358, no. 5, pp. 502–511, 2008. View at Publisher · View at Google Scholar · View at Scopus
  16. E. Córdova-Alarcón, F. Centeno, J. Reyes-Esparza, A. García-Carrancá, and E. Garrido, “Effects of HRAS oncogene on cell cycle progression in a cervical cancer-derived cell line,” Archives of Medical Research, vol. 36, no. 4, pp. 311–316, 2005. View at Publisher · View at Google Scholar · View at Scopus
  17. Y. Li, F. Wang, J. Xu et al., “Progressive miRNA expression profiles in cervical carcinogenesis and identification of HPV-related target genes for miR-29,” Journal of Pathology, vol. 224, no. 4, pp. 484–495, 2011. View at Publisher · View at Google Scholar · View at Scopus
  18. W.-O. Lui, N. Pourmand, B. K. Patterson, and A. Fire, “Patterns of known and novel small RNAs in human cervical cancer,” Cancer Research, vol. 67, no. 13, pp. 6031–6043, 2007. View at Publisher · View at Google Scholar · View at Scopus
  19. 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
  20. P. Dufourcq, L. Leroux, J. Ezan et al., “Regulation of endothelial cell cytoskeletal reorganization by a secreted frizzled-related protein-1 and frizzled 4- and frizzled 7-dependent pathway: role in neovessel formation,” American Journal of Pathology, vol. 172, no. 1, pp. 37–49, 2008. View at Publisher · View at Google Scholar · View at Scopus
  21. E. Minet, G. Michel, D. Mottet et al., “C-JUN gene induction and AP-1 activity is regulated by a JNK-dependent pathway in hypoxic HepG2 cells,” Experimental Cell Research, vol. 265, no. 1, pp. 114–124, 2001. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Manavi, G. Hudelist, A. F. Retter, D. K. Gschwandtler, K. Pischinger, and K. Czerwenka, “Gene profiling in Pap-cell smears of high-risk human papillomavirus-positive squamous cervical carcinoma,” Gynecologic Oncology, vol. 105, no. 2, pp. 418–426, 2007. View at Publisher · View at Google Scholar · View at Scopus
  23. F. Kottakis, C. Polytarchou, P. Foltopoulou, I. Sanidas, S. C. Kampranis, and P. N. Tsichlis, “FGF-2 regulates cell proliferation, migration, and angiogenesis through an NDY1/KDM2B-miR-101-EZH2 pathway,” Molecular Cell, vol. 43, no. 2, pp. 285–298, 2011. View at Publisher · View at Google Scholar · View at Scopus
  24. S. Varambally, Q. Cao, R.-S. Mani et al., “Genomic loss of microRNA-101 leads to overexpression of histone methyltransferase EZH2 in cancer,” Science, vol. 322, no. 5908, pp. 1695–1699, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. J. Fang, M. Zhang, and Q. Li, “Enhancer of zeste homolog 2 expression is associated with tumor cell proliferation and invasion in cervical cancer,” American Journal of the Medical Sciences, vol. 342, no. 3, pp. 198–204, 2011. View at Publisher · View at Google Scholar · View at Scopus
  26. H. Moore, M. Gonzalez, K. Toy, A. M. Cimino, P. Argani, and C. Kleer, “EZH2 inhibition decreases p38 signaling and suppresses breast cancer motility and metastasis,” Breast Cancer Research and Treatment, vol. 138, no. 3, pp. 741–752, 2013. View at Publisher · View at Google Scholar
  27. E. Vire, C. Brenner, R. Deplus et al., “The Polycomb group protein EZH2 directly controls DNA methylation,” Nature, vol. 439, pp. 871–874, 2006. View at Google Scholar
  28. D. Holland, K. S. Hoppe, B. Schuller et al., “Activation of the enhancer of zeste homologue 2 gene by the human papillomavirus E7 oncoprotein,” Cancer Research, vol. 68, no. 23, pp. 9964–9972, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. M. Negrini and G. A. Calin, “Breast cancer metastasis: a microRNA story,” Breast Cancer Research, vol. 10, no. 2, article 303, 2008. View at Publisher · View at Google Scholar · View at Scopus
  30. I. Martinez, A. S. Gardiner, K. F. Board, F. A. Monzon, R. P. Edwards, and S. A. Khan, “Human papillomavirus type 16 reduces the expression of microRNA-218 in cervical carcinoma cells,” Oncogene, vol. 27, no. 18, pp. 2575–2582, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. B. Liu, X. C. Peng, X. L. Zheng, J. Wang, and Y. W. Qin, “MiR-126 restoration down-regulate VEGF and inhibit the growth of lung cancer cell lines in vitro and in vivo,” Lung Cancer, vol. 66, no. 2, pp. 169–175, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. D. K. Gaffney, D. Haslam, A. Tsodikov et al., “Epidermal growth factor receptor (EGFR) and vascular endothelial growth factor (VEGF) negatively affect overall survival in carcinoma of the cervix treated with radiotherapy,” International Journal of Radiation Oncology Biology Physics, vol. 56, no. 4, pp. 922–928, 2003. View at Publisher · View at Google Scholar · View at Scopus
  33. X. Wang and C. Tournier, “Regulation of cellular functions by the ERK5 signalling pathway,” Cellular Signalling, vol. 18, no. 6, pp. 753–760, 2006. View at Publisher · View at Google Scholar · View at Scopus
  34. Y. Li, M. Zhang, H. Chen et al., “Ratio of miR-196s to HOXC8 messenger RNA correlates with breast cancer cell migration and metastasis,” Cancer Research, vol. 70, no. 20, pp. 7894–7904, 2010. View at Publisher · View at Google Scholar · View at Scopus
  35. C. How, A. Hui, P. Boutros et al., “microRNA-196b regulates HOXB7 in cervical cancer,” Cancer Research, vol. 72, no. 8, supplement, abstract 2311, pp. 1538–7445, 2012, Proceedings of the 103rd Annual Meeting of the American Association for Cancer Research, 2012. View at Publisher · View at Google Scholar
  36. C. How, A. B. Hui, A. W. Fyles, and F. F. Liu, “The role of microRNA-196b in cervical cancer,” Cancer Research, vol. 70, no. 8, supplement 1, abstract 2059, 2010, Proceedings of the 101st Annual Meeting of the American Association for Cancer Research, 2010. View at Publisher · View at Google Scholar
  37. A. Uesugi, K.-I. Kozaki, T. Tsuruta et al., “The tumor suppressive microRNA miR-218 targets the mTOR component rictor and inhibits AKT phosphorylation in oral cancer,” Cancer Research, vol. 71, no. 17, pp. 5765–5778, 2011. View at Publisher · View at Google Scholar · View at Scopus
  38. D. W. Wu, Y. W. Cheng, J. Wang, C. Y. Chen, and H. Lee, “Paxillin predicts survival and relapse in non-small cell lung cancer by microRNA-218 targeting,” Cancer Research, vol. 70, no. 24, pp. 10392–10401, 2010. View at Publisher · View at Google Scholar · View at Scopus
  39. S. Tatarano, T. Chiyomaru, K. Kawakami et al., “miR-218 on the genomic loss region of chromosome 4p15.31 functions as a tumor suppressor in bladder cancer,” International Journal of Oncology, vol. 39, no. 1, pp. 13–21, 2011. View at Publisher · View at Google Scholar · View at Scopus
  40. J. Tie, Y. Pan, L. Zhao et al., “MiR-218 inhibits invasion and metastasis of gastric cancer by targeting the robo1 receptor,” PLoS Genetics, vol. 6, no. 3, Article ID e1000879, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. J. A. Legg, J. M. J. Herbert, P. Clissold, and R. Bicknell, “Slits and Roundabouts in cancer, tumour angiogenesis and endothelial cell migration,” Angiogenesis, vol. 11, no. 1, pp. 13–21, 2008. View at Publisher · View at Google Scholar · View at Scopus
  42. B. Wang, Y. Xiao, B. B. Ding et al., “Induction of tumor angiogenesis by Slit-Robo signaling and inhibition of cancer growth by blocking Robo activity,” Cancer Cell, vol. 4, no. 1, pp. 19–29, 2003. View at Publisher · View at Google Scholar · View at Scopus
  43. A. S. Gardiner, W. C. McBee, Jr. et al., “MicroRNA analysis in human papillomavirus (HPV)-associated cervical neoplasia and cancer,” Journal Carcinogene Mutagene, vol. 5, supplement 1, article A55, 2011. View at Publisher · View at Google Scholar
  44. J. Yu, Y. Wang, R. Dong, X. Huang, S. Ding, and H. Qiu, “Circulating microRNA-218 was reduced in cervical cancer and correlated with tumor invasion,” Journal of Cancer Research and Clinical Oncology, vol. 138, no. 4, pp. 671–674, 2012. View at Publisher · View at Google Scholar · View at Scopus
  45. A. R. R. Forrest, M. K. Kanamori, Y. Tomaru et al., “Induction of microRNAs, mir-155, mir-222, mir-424 and mir-503, promotes monocytic differentiation through combinatorial regulation,” Leukemia, vol. 24, no. 2, pp. 460–466, 2010. View at Publisher · View at Google Scholar · View at Scopus
  46. C. P. Pallasch, M. Patz, J. P. Yoon et al., “miRNA deregulation by epigenetic silencing disrupts suppression of the oncogene PLAG1 in chronic lymphocytic leukemia,” Blood, vol. 114, no. 15, pp. 3255–3264, 2009. View at Publisher · View at Google Scholar · View at Scopus
  47. J. Xu, Y. Li, F. Wang et al., “Suppressed miR-424 expression via upregulation of target gene Chk1 contributes to the progression of cervical cancer,” Oncogene, 2012. View at Publisher · View at Google Scholar · View at Scopus
  48. G. Zachos, M. D. Rainey, and D. A. F. Gillespie, “Chk1-deficient tumour cells are viable but exhibit multiple checkpoint and survival defects,” EMBO Journal, vol. 22, no. 3, pp. 713–723, 2003. View at Publisher · View at Google Scholar · View at Scopus
  49. S. Volinia, G. A. Calin, C.-G. Liu et al., “A microRNA expression signature of human solid tumors defines cancer gene targets,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 7, pp. 2257–2261, 2006. View at Publisher · View at Google Scholar · View at Scopus
  50. P. M. Pereira, J. P. Marques, A. R. Soares, L. Carreto, and M. A. S. Santos, “Microrna expression variability in human cervical tissues,” PLoS One, vol. 5, no. 7, Article ID e11780, 2010. View at Publisher · View at Google Scholar · View at Scopus
  51. M.-J. Long, F.-X. Wu, P. Li, M. Liu, X. Li, and H. Tang, “MicroRNA-10a targets CHL1 and promotes cell growth, migration and invasion in human cervical cancer cells,” Cancer Letters, vol. 324, pp. 186–196, 2012. View at Publisher · View at Google Scholar
  52. J.-G. Zhang, J.-J. Wang, F. Zhao, Q. Liu, K. Jiang, and G. H. Yang, “MicroRNA-21 (miR-21) represses tumor suppressor PTEN and promotes growth and invasion in non-small cell lung cancer (NSCLC),” Clinica Chimica Acta International Journal of Clinical Chemistry, vol. 411, no. 11-12, pp. 846–852, 2010. View at Google Scholar · View at Scopus
  53. A. B. Y. Hui, M. Lenarduzzi, T. Krushel et al., “Comprehensive MicroRNA profiling for head and neck squamous cell carcinomas,” Clinical Cancer Research, vol. 16, no. 4, pp. 1129–1139, 2010. View at Publisher · View at Google Scholar · View at Scopus
  54. F. Meng, R. Henson, H. J. Wehbe, K. Ghoshal, S. T. Jacob, and T. Patel, “MicroRNA-21 regulates expression of the PTEN tumor suppressor gene in human hepatocellular cancer,” Gastroenterology, vol. 133, no. 2, pp. 647–658, 2007. View at Publisher · View at Google Scholar · View at Scopus
  55. Y. Zhai, K. B. Hotary, B. Nan et al., “Expression of membrane type 1 matrix metalloproteinase is associated with cervical carcinoma progression and invasion,” Cancer Research, vol. 65, no. 15, pp. 6543–6550, 2005. View at Publisher · View at Google Scholar · View at Scopus
  56. T. Hagemann, T. Bozanovic, S. Hooper et al., “Molecular profiling of cervical cancer progression,” British Journal of Cancer, vol. 96, no. 2, pp. 321–328, 2007. View at Publisher · View at Google Scholar · View at Scopus
  57. S. Zhu, M. L. Si, H. Wu, and Y. Y. Mo, “MicroRNA-21 targets the tumor suppressor gene tropomyosin 1 (TPM1),” Journal of Biological Chemistry, vol. 282, no. 19, pp. 14328–14336, 2007. View at Publisher · View at Google Scholar · View at Scopus
  58. S. Zhu, H. Wu, F. Wu, D. Nie, S. Sheng, and Y. Y. Mo, “MicroRNA-21 targets tumor suppressor genes in invasion and metastasis,” Cell Research, vol. 18, no. 3, pp. 350–359, 2008. View at Publisher · View at Google Scholar · View at Scopus
  59. Y.-F. Wong, T.-H. Cheung, G. S. W. Tsao et al., “Genome-wide gene expression profiling of cervical cancer in Hong Kong women by oligonucleotide microarray,” International Journal of Cancer, vol. 118, no. 10, pp. 2461–2469, 2006. View at Publisher · View at Google Scholar · View at Scopus
  60. Q. Yao, H. Xu, Q. Q. Zhang, H. Zhou, and L. H. Qu, “MicroRNA-21 promotes cell proliferation and down-regulates the expression of programmed cell death 4 (PDCD4) in HeLa cervical carcinoma cells,” Biochemical and Biophysical Research Communications, vol. 388, no. 3, pp. 539–542, 2009. View at Publisher · View at Google Scholar · View at Scopus
  61. S. Pan, F. Yu, C. Gong, and E. Song, “Tumor invasion and metastasis initiated by mir-106b in breast cancer by targeting BRMS1 and RB,” Cancer Research, vol. 69, no. 24, supplement, 2009, Proceedings of the 32nd Annual CTRC-AACR San Antonio Breast Cancer Symposium, 2009. View at Publisher · View at Google Scholar
  62. A. Shai, T. Brake, C. Somoza, and P. F. Lambert, “The human papillomavirus E6 oncogene dysregulates the cell cycle and contributes to cervical carcinogenesis through two independent activities,” Cancer Research, vol. 67, no. 4, pp. 1626–1635, 2007. View at Publisher · View at Google Scholar · View at Scopus
  63. S. Balsitis, F. Dick, N. Dyson, and P. F. Lambert, “Critical roles for non-pRb targets of human papillomavirus type 16 E7 in cervical carcinogenesis,” Cancer Research, vol. 66, no. 19, pp. 9393–9400, 2006. View at Publisher · View at Google Scholar · View at Scopus
  64. T. Araki and J. Milbrandt, “Ninjurin2, a novel homophilic adhesion molecule, is expressed in mature sensory and enteric neurons and promotes neurite outgrowth,” Journal of Neuroscience, vol. 20, no. 1, pp. 187–195, 2000. View at Google Scholar · View at Scopus
  65. D. Gius, M. C. Funk, E. Y. Chuang et al., “Profiling microdissected epithelium and stroma to model genomic signatures for cervical carcinogenesis accommodating for covariates,” Cancer Research, vol. 67, no. 15, pp. 7113–7123, 2007. View at Publisher · View at Google Scholar · View at Scopus
  66. Y. X. Wang, X. Y. Zhang, B. F. Zhang, C. Q. Yang, X. M. Chen, and H. J. Gao, “Initial study of microRNA expression profiles of colonic cancer without lymph node metastasis,” Journal of Digestive Diseases, vol. 11, no. 1, pp. 50–54, 2010. View at Publisher · View at Google Scholar · View at Scopus
  67. P. Descargues, C. Draison, C. Bonnart et al., “Spink5-deficient mice mimic Netherton syndrome through degradation of desmoglein 1 by epidermal protease hyperactivity,” Nature Genetics, vol. 37, no. 1, pp. 56–65, 2005. View at Publisher · View at Google Scholar · View at Scopus
  68. J.-W. Lee, Y.-A. Park, J.-J. Choi et al., “The expression of the miRNA-200 family in endometrial endometrioid carcinoma,” Gynecologic Oncology, vol. 120, no. 1, pp. 56–62, 2011. View at Publisher · View at Google Scholar · View at Scopus
  69. K. P. Porkka, M. J. Pfeiffer, K. K. Waltering, R. L. Vessella, T. L. J. Tammela, and T. Visakorpi, “MicroRNA expression profiling in prostate cancer,” Cancer Research, vol. 67, no. 13, pp. 6130–6135, 2007. View at Publisher · View at Google Scholar · View at Scopus
  70. M. V. Iorio, R. Visone, G. Di Leva et al., “MicroRNA signatures in human ovarian cancer,” Cancer Research, vol. 67, no. 18, pp. 8699–8707, 2007. View at Publisher · View at Google Scholar · View at Scopus
  71. B. Wang, P. Koh, C. Winbanks et al., “MiR-200a prevents renal fibrogenesis through repression of TGF-β2 expression,” Diabetes, vol. 60, no. 1, pp. 280–287, 2011. View at Publisher · View at Google Scholar · View at Scopus
  72. X.-C. Xu, M. F. Mitchell, E. Silva, A. Jetten, and R. Lotan, “Decreased expression of retinoic acid receptors, transforming growth factor β, involucrin, and cornifin in cervical intraepithelial neoplasia,” Clinical Cancer Research, vol. 5, no. 6, pp. 1503–1508, 1999. View at Google Scholar · View at Scopus
  73. A. Budhu, J. Ji, and X. W. Wang, “The clinical potential of microRNAs,” Journal of Hematology and Oncology, vol. 3, article 37, 2010. View at Publisher · View at Google Scholar · View at Scopus
  74. S.-L. Guo, Z. Peng, X. Yang et al., “mir-148a promoted cell proliferation by targeting p27 in gastric cancer cells,” International Journal of Biological Sciences, vol. 7, no. 5, pp. 567–574, 2011. View at Google Scholar · View at Scopus
  75. G. V. De Putte, R. Holm, A. K. Lie, C. G. Tropé, and G. B. Kristensen, “Expression of p27, p21, and p16 protein in early squamous cervical cancer and its relation to prognosis,” Gynecologic Oncology, vol. 89, no. 1, pp. 140–147, 2003. View at Publisher · View at Google Scholar · View at Scopus
  76. S. Bernard and M. Eilers, “Control of cell proliferation and growth by Myc proteins,” Results and Problems in Cell Differentiation, vol. 42, pp. 329–342, 2006. View at Publisher · View at Google Scholar · View at Scopus
  77. Z. Zhang, H. Sun, H. Dai et al., “MicroRNA miR-210 modulates cellular response to hypoxia through the MYC antagonist MNT,” Cell Cycle, vol. 8, no. 17, pp. 2756–2768, 2009. View at Google Scholar · View at Scopus
  78. D. A. Arvanitis and D. A. Spandidos, “Deregulation of the G1/S phase transition in cancer and squamous intraepithelial lesions of the uterine cervix: a case control study,” Oncology Reports, vol. 20, no. 4, pp. 751–760, 2008. View at Publisher · View at Google Scholar · View at Scopus
  79. H. Yang, W. Kong, L. He et al., “MicroRNA expression profiling in human ovarian cancer: miR-214 induces cell survival and cisplatin resistance by targeting PTEN,” Cancer Research, vol. 68, pp. 425–433, 2008. View at Google Scholar
  80. J.-W. Lee, C. H. Choi, J.-J. Choi et al., “Altered MicroRNA expression in cervical carcinomas,” Clinical Cancer Research, vol. 14, no. 9, pp. 2535–2542, 2008. View at Publisher · View at Google Scholar · View at Scopus
  81. J. S. Lee, Y. D. Choi, J. H. Lee et al., “Expression of PTEN in the progression of cervical neoplasia and its relation to tumor behavior and angiogenesis in invasive squamous cell carcinoma,” Journal of Surgical Oncology, vol. 93, no. 3, pp. 233–240, 2006. View at Publisher · View at Google Scholar · View at Scopus
  82. Y. Y. Ma, S. J. Wei, Y. C. Lin et al., “PIK3CA as an oncogene in cervical cancer,” Oncogene, vol. 19, no. 23, pp. 2739–2744, 2000. View at Google Scholar · View at Scopus
  83. C.-Z. Chen, L. Li, H. F. Lodish, and D. P. Bartel, “MicroRNAs modulate hematopoietic lineage differentiation,” Science, vol. 303, no. 5654, pp. 83–86, 2004. View at Publisher · View at Google Scholar · View at Scopus
  84. H. Wan, M. Yuan, C. Simpson et al., “Stem/progenitor cell-like properties of desmoglein 3dim cells in primary and immortalized keratinocyte lines,” Stem Cells, vol. 25, no. 5, pp. 1286–1297, 2007. View at Publisher · View at Google Scholar · View at Scopus
  85. A. Bernards and J. Settleman, “Loss of the ras regulator RASAL1: another route to ras activation in colorectal cancer,” Gastroenterology, vol. 136, no. 1, pp. 46–48, 2009. View at Publisher · View at Google Scholar · View at Scopus
  86. Z. M. Zheng and C. C. Baker, “Papillomavirus genome structure, expression, and post-transcriptional regulation,” Frontiers in Bioscience, vol. 11, no. 1, pp. 2286–2302, 2006. View at Publisher · View at Google Scholar · View at Scopus
  87. A. Berrington De González and J. Green, “Comparison of risk factors for invasive squamous cell carcinoma and adenocarcinoma of the cervix: Collaborative reanalysis of individual data on 8, 097 women with squamous cell carcinoma and 1, 374 women with adenocarcinoma from 12 epidemiological studies,” International Journal of Cancer, vol. 120, pp. 885–891, 2007. View at Google Scholar
  88. X. Castellsagué, M. Diaz, S. de Sanjosé et al., “Worldwide human papillomavirus etiology of cervical adenocarcinoma and its cofactors: implications for screening and prevention,” Journal of the National Cancer Institute, vol. 98, no. 5, pp. 303–315, 2006. View at Publisher · View at Google Scholar · View at Scopus
  89. X. Wang, H. K. Wang, J. P. Mccoy et al., “Oncogenic HPV infection interrupts the expression of tumor-suppressive miR-34a through viral oncoprotein E6,” RNA, vol. 15, no. 4, pp. 637–647, 2009. View at Publisher · View at Google Scholar · View at Scopus
  90. E. C. Thorland, S. L. Myers, B. S. Gostout, and D. I. Smith, “Common fragile sites are preferential targets for HPV16 integrations in cervical tumors,” Oncogene, vol. 22, no. 8, pp. 1225–1237, 2003. View at Publisher · View at Google Scholar · View at Scopus
  91. T. Yao and Z. Lin, “MiR-21 is involved in cervical squamous cell tumorigenesis and regulates CCL20,” Biochimica et Biophysica Acta, vol. 1822, no. 2, pp. 248–260, 2012. View at Publisher · View at Google Scholar · View at Scopus
  92. Y. Nominé, M. Masson, S. Charbonnier et al., “Structural and functional analysis of E6 oncoprotein: insights in the molecular pathways of human papillomavirus-mediated pathogenesis,” Molecular Cell, vol. 21, no. 5, pp. 665–678, 2006. View at Publisher · View at Google Scholar · View at Scopus
  93. C. L. Au Yeung, T. Y. Tsang, P. L. Yau, and T. T. Kwok, “Human papillomavirus type 16 E6 induces cervical cancer cell migration through the p53/microRNA-23b/urokinase-type plasminogen activator pathway,” Oncogene, vol. 30, no. 21, pp. 2401–2410, 2011. View at Publisher · View at Google Scholar · View at Scopus
  94. M. J. Duffy, T. M. Maguire, E. W. McDermott, and N. O. 'Higgins, “Urokinase plasminogen activator: a prognostic marker in multiple types of cancer,” Journal of Surgical Oncology, vol. 71, no. 2, pp. 130–135, 1999. View at Google Scholar
  95. L. Riethdorf, S. Riethdorf, S. Petersen et al., “Urokinase gene expression indicates early invasive growth in squamous cell lesions of the uterine cervix,” The Journal of Pathology, vol. 189, no. 2, pp. 245–250, 1999. View at Google Scholar
  96. T.-C. Chang, E. A. Wentzel, O. A. Kent et al., “Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis,” Molecular Cell, vol. 26, no. 5, pp. 745–752, 2007. View at Publisher · View at Google Scholar · View at Scopus
  97. N. Raver-Shapira, E. Marciano, E. Meiri et al., “Transcriptional activation of miR-34a contributes to p53-mediated apoptosis,” Molecular Cell, vol. 26, no. 5, pp. 731–743, 2007. View at Publisher · View at Google Scholar · View at Scopus
  98. F. Sun, H. Fu, Q. Liu et al., “Downregulation of CCND1 and CDK6 by miR-34a induces cell cycle arrest,” FEBS Letters, vol. 582, no. 10, pp. 1564–1568, 2008. View at Publisher · View at Google Scholar · View at Scopus
  99. X. Wang, C. Meyers, M. Guo, and Z. M. Zheng, “Upregulation of p18Ink4c expression by oncogenic HPV E6 via p53-miR-34a pathway,” International Journal of Cancer, vol. 129, no. 6, pp. 1362–1372, 2011. View at Publisher · View at Google Scholar · View at Scopus
  100. M. P. Myklebust, O. Bruland, O. Fluge, A. Skarstein, L. Balteskard, and O. Dahl, “MicroRNA-15b is induced with E2F-controlled genes in HPV-related cancer,” British Journal of Cancer, vol. 105, no. 11, pp. 1719–1725, 2011. View at Publisher · View at Google Scholar · View at Scopus
  101. S. L. Gonzalez, M. Stremlau, X. He, J. R. Basile, and K. Münger, “Degradation of the retinoblastoma tumor suppressor by the human papillomavirus type 16 E7 oncoprotein is important for functional inactivation and is separable from proteasomal degradation of E7,” Journal of Virology, vol. 75, no. 16, pp. 7583–7591, 2001. View at Publisher · View at Google Scholar · View at Scopus
  102. N. Dyson, P. M. Howley, K. Munger, and E. Harlow, “The human papilloma virus-16 E7 oncoprotein is able to bind to the retinoblastoma gene product,” Science, vol. 243, no. 4893, pp. 934–937, 1989. View at Google Scholar · View at Scopus
  103. M. Ofir, D. Hacohen, and D. Ginsberg, “miR-15 and miR-16 are direct transcriptional targets of E2F1 that limit E2F-induced proliferation by targeting cyclin E,” Molecular Cancer Research, vol. 9, no. 4, pp. 440–447, 2011. View at Publisher · View at Google Scholar · View at Scopus
  104. M. J. Bueno, M. G. De Cedrón, U. Laresgoiti, J. Fernández-Piqueras, A. M. Zubiaga, and M. Malumbres, “Multiple E2F-induced microRNAs prevent replicative stress in response to mitogenic signaling,” Molecular and Cellular Biology, vol. 30, no. 12, pp. 2983–2995, 2010. View at Publisher · View at Google Scholar · View at Scopus
  105. L. B. da Silva Cardeal, E. Boccardo, L. Termini et al., “HPV16 oncoproteins induce MMPs/RECK-TIMP-2 imbalance in primary keratinocytes: possible implications in cervical carcinogenesis,” PLoS One, vol. 7, no. 3, Article ID e33585, 2012. View at Publisher · View at Google Scholar · View at Scopus
  106. S. Takagi, S. Simizu, and H. Osada, “Reck negatively regulates matrix metalloproteinase-9 transcription,” Cancer Research, vol. 69, no. 4, pp. 1502–1508, 2009. View at Publisher · View at Google Scholar · View at Scopus
  107. R. M. Sasahara, S. M. Brochado, C. Takahashi et al., “Transcriptional control of the RECK metastasis/angiogenesis suppressor gene,” Cancer Detection and Prevention, vol. 26, no. 6, pp. 435–443, 2002. View at Publisher · View at Google Scholar · View at Scopus
  108. R. Yi, M. N. Poy, M. Stoffel, and E. Fuchs, “A skin microRNA promotes differentiation by repressing ‘stemness’,” Nature, vol. 452, no. 7184, pp. 225–229, 2008. View at Publisher · View at Google Scholar · View at Scopus
  109. M. Melar-New and L. A. Laimins, “Human papillomaviruses modulate expression of microRNA 203 upon epithelial differentiation to control levels of p63 proteins,” Journal of Virology, vol. 84, no. 10, pp. 5212–5221, 2010. View at Publisher · View at Google Scholar · View at Scopus
  110. A. M. Lena, R. Shalom-Feuerstein, P. R. di Val Cervo et al., “miR-203 represses “stemness” by repressing ΔNp63,” Cell Death and Differentiation, vol. 15, no. 7, pp. 1187–1195, 2008. View at Publisher · View at Google Scholar · View at Scopus
  111. A. B. Truong, M. Kretz, T. W. Ridky, R. Kimmel, and P. A. Khavari, “p63 regulates proliferation and differentiation of developmentally mature keratinocytes,” Genes and Development, vol. 20, no. 22, pp. 3185–3197, 2006. View at Publisher · View at Google Scholar · View at Scopus
  112. D. Spitkovsky, S. P. Hehner, T. G. Hofmann, A. Möller, and M. Lienhard Schmitz, “The human papillomavirus oncoprotein E7 attenuates NF-κB activation by targeting the IκB kinase complex,” Journal of Biological Chemistry, vol. 277, no. 28, pp. 25576–25582, 2002. View at Publisher · View at Google Scholar · View at Scopus
  113. D. J. McKenna, S. S. McDade, D. Patel, and D. J. McCance, “MicroRNA 203 expression in keratinocytes is dependent on regulation of p53 levels by E6,” Journal of Virology, vol. 84, no. 20, pp. 10644–10652, 2010. View at Publisher · View at Google Scholar · View at Scopus
  114. E. Ferretti, E. De Smaele, A. Po et al., “MicroRNA profiling in human medulloblastoma,” International Journal of Cancer, vol. 124, no. 3, pp. 568–577, 2009. View at Publisher · View at Google Scholar · View at Scopus
  115. A. Gaur, D. A. Jewell, Y. Liang et al., “Characterization of microRNA expression levels and their biological correlates in human cancer cell lines,” Cancer Research, vol. 67, no. 6, pp. 2456–2468, 2007. View at Publisher · View at Google Scholar · View at Scopus
  116. T. Katada, H. Ishiguro, Y. Kuwabara et al., “MicroRNA expression profile in undifferentiated gastric cancer,” International Journal of Oncology, vol. 34, no. 2, pp. 537–542, 2009. View at Publisher · View at Google Scholar · View at Scopus
  117. E. Bandrés, E. Cubedo, X. Agirre et al., “Identification by Real-time PCR of 13 mature microRNAs differentially expressed in colorectal cancer and non-tumoral tissues,” Molecular Cancer, vol. 5, article 29, 2006. View at Publisher · View at Google Scholar · View at Scopus
  118. W. Kong, H. Yang, L. He et al., “MicroRNA-155 is regulated by the transforming growth factor β/Smad pathway and contributes to epithelial cell plasticity by targeting RhoA,” Molecular and Cellular Biology, vol. 28, no. 22, pp. 6773–6784, 2008. View at Publisher · View at Google Scholar · View at Scopus
  119. M. Perez-Moreno, C. Jamora, and E. Fuchs, “Sticky business: orchestrating cellular signals at adherens junctions,” Cell, vol. 112, no. 4, pp. 535–548, 2003. View at Publisher · View at Google Scholar · View at Scopus
  120. O. Peralta-Zaragoza, V. Bermúdez-Morales, L. Gutiérrez-Xicotencatl, J. Alcocer-González, F. Recillas-Targa, and V. Madrid-Marina, “E6 and E7 oncoproteins from human papillomavirus type 16 induce activation of human transforming growth factor β1 promoter throughout Sp1 recognition sequence,” Viral Immunology, vol. 19, no. 3, pp. 468–480, 2006. View at Publisher · View at Google Scholar · View at Scopus
  121. M. G. Noordhuis, R. S. N. Fehrmann, G. B. A. Wisman et al., “Involvement of the TGF-β and β-catenin pathways in pelvic lymph node metastasis in early-stage cervical cancer,” Clinical Cancer Research, vol. 17, no. 6, pp. 1317–1330, 2011. View at Publisher · View at Google Scholar · View at Scopus
  122. W. S. Ahn, S. M. Bae, J. M. Lee et al., “Searching for pathogenic gene functions to cervical cancer,” Gynecologic Oncology, vol. 93, no. 1, pp. 41–48, 2004. View at Publisher · View at Google Scholar · View at Scopus
  123. M. V. Iorio, M. Ferracin, C. G. Liu et al., “MicroRNA gene expression deregulation in human breast cancer,” Cancer Research, vol. 65, no. 16, pp. 7065–7070, 2005. View at Publisher · View at Google Scholar · View at Scopus
  124. J. P. Maufort, A. Shai, H. C. Pitot, and P. F. Lambert, “A role for HPV16 E5 in cervical carcinogenesis,” Cancer Research, vol. 70, no. 7, pp. 2924–2931, 2010. View at Publisher · View at Google Scholar · View at Scopus
  125. N. Kivi, D. Greco, P. Auvinen, and E. Auvinen, “Genes involved in cell adhesion, cell motility and mitogenic signaling are altered due to HPV 16 E5 protein expression,” Oncogene, vol. 27, no. 18, pp. 2532–2541, 2008. View at Publisher · View at Google Scholar · View at Scopus
  126. R. R. Riley, S. Duensing, T. Brake, K. Münger, P. F. Lambert, and J. M. Arbeit, “Dissection of human papillomavirus E6 and E7 function in transgenic mouse models of cervical carcinogenesis,” Cancer Research, vol. 63, no. 16, pp. 4862–4871, 2003. View at Google Scholar · View at Scopus
  127. D. Greco, N. Kivi, K. Qian, S.-K. Leivonen, P. Auvinen, and E. Auvinen, “Human papillomavirus 16 E5 modulates the expression of host microRNAS,” PLoS One, vol. 6, no. 7, Article ID e21646, 2011. View at Publisher · View at Google Scholar · View at Scopus
  128. P. J. B. Sabatini, M. Zhang, R. Silverman-Gavrila, M. P. Bendeck, and B. L. Langille, “Homotypic and endothelial cell adhesions via N-cadherin determine polarity and regulate migration of vascular smooth muscle cells,” Circulation Research, vol. 103, no. 4, pp. 405–412, 2008. View at Publisher · View at Google Scholar · View at Scopus
  129. 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
  130. D. Pim, M. Bergant, S. S. Boon et al., “Human papillomaviruses and the specificity of PDZ domain targeting,” The FEBS Journal, vol. 279, no. 19, pp. 3530–3537, 2012. View at Publisher · View at Google Scholar
  131. M. P. Gantier, C. E. McCoy, I. Rusinova et al., “Analysis of microRNA turnover in mammalian cells following Dicer1 ablation,” Nucleic Acids Research, vol. 39, no. 13, pp. 5692–5703, 2011. View at Publisher · View at Google Scholar · View at Scopus
  132. X. Chen, Y. Ba, L. Ma et al., “Characterization of microRNAs in serum: a novel class of biomarkers for diagnosis of cancer and other diseases,” Cell Research, vol. 18, no. 10, pp. 997–1006, 2008. View at Publisher · View at Google Scholar · View at Scopus
  133. J. Li, P. Smyth, R. Flavin et al., “Comparison of miRNA expression patterns using total RNA extracted from matched samples of formalin-fixed paraffin-embedded (FFPE) cells and snap frozen cells,” BMC Biotechnology, vol. 7, article 36, 2007. View at Publisher · View at Google Scholar · View at Scopus
  134. J.-W. Lee, C. H. Choi, J. J. Choi et al., “Altered microRNA expression in cervical carcinomas,” Clinical Cancer Research, vol. 14, no. 9, pp. 2535–2542, 2008. View at Publisher · View at Google Scholar · View at Scopus
  135. G. A. Calin, M. Ferracin, A. Cimmino et al., “A microRNA signature associated with prognosis and progression in chronic lymphocytic leukemia,” The New England Journal of Medicine, vol. 353, no. 17, pp. 1793–1801, 2005. View at Publisher · View at Google Scholar · View at Scopus
  136. C. Roldo, E. Missiaglia, J. P. Hagan et al., “MicroRNA expression abnormalities in pancreatic endocrine and acinar tumors are associated with distinctive pathologic features and clinical behavior,” Journal of Clinical Oncology, vol. 24, no. 29, pp. 4677–4684, 2006. View at Publisher · View at Google Scholar · View at Scopus
  137. C. Blenkiron, L. D. Goldstein, N. P. Thorne et al., “MicroRNA expression profiling of human breast cancer identifies new markers of tumor subtype,” Genome Biology, vol. 8, no. 10, article R214, 2007. View at Publisher · View at Google Scholar · View at Scopus
  138. M. Raponi, L. Dossey, T. Jatkoe et al., “MicroRNA classifiers for predicting prognosis of squamous cell lung cancer,” Cancer Research, vol. 69, no. 14, pp. 5776–5783, 2009. View at Publisher · View at Google Scholar · View at Scopus
  139. X. Hu, J. K. Schwarz, J. S. Lewis Jr. et al., “A microRNA expression signature for cervical cancer prognosis,” Cancer Research, vol. 70, no. 4, pp. 1441–1448, 2010. View at Publisher · View at Google Scholar · View at Scopus
  140. M. G. V. Heiden, L. C. Cantley, and C. B. Thompson, “Understanding the warburg effect: the metabolic requirements of cell proliferation,” Science, vol. 324, no. 5930, pp. 1029–1033, 2009. View at Publisher · View at Google Scholar · View at Scopus
  141. 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