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International Journal of Hepatology
Volume 2014, Article ID 791045, 10 pages
http://dx.doi.org/10.1155/2014/791045
Research Article

Circulating MicroRNAs in Plasma of Hepatitis B e Antigen Positive Children Reveal Liver-Specific Target Genes

1Department of Paediatrics, Hvidovre Hospital, University of Copenhagen, Kettegaard Allé 30, 2650 Hvidovre, Denmark
2Department of Paediatrics and Center for Non-Coding RNA in Technology and Health, Herlev Hospital, University of Copenhagen, Arkaden, 2730 Herlev, Denmark

Received 27 August 2014; Accepted 19 November 2014; Published 17 December 2014

Academic Editor: Daisuke Morioka

Copyright © 2014 Thilde Nordmann Winther 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. M.-W. Yu, H.-C. Chang, Y.-F. Liaw et al., “Familial risk of hepatocellular carcinoma among chronic hepatitis B carriers and their relatives,” Journal of the National Cancer Institute, vol. 92, no. 14, pp. 1159–1164, 2000. View at Publisher · View at Google Scholar · View at Scopus
  2. Z. Luo, L. Li, and B. Ruan, “Impact of the implementation of a vaccination strategy on hepatitis B virus infections in China over a 20-year period,” International Journal of Infectious Diseases, vol. 16, no. 2, pp. e82–e88, 2012. View at Publisher · View at Google Scholar · View at Scopus
  3. Y.-F. Wei, G.-Y. Cui, P. Ye, J.-N. Chen, and H.-Y. Diao, “MicroRNAs may solve the mystery of chronic hepatitis B virus infection,” World Journal of Gastroenterology, vol. 19, no. 30, pp. 4867–4876, 2013. View at Publisher · View at Google Scholar · View at Scopus
  4. T. N. Winther, C. H. Bang-Berthelsen, I. L. Heiberg, F. Pociot, and B. Hogh, “Differential plasma microRNA profiles in HBeAg positive and HBeAg negative children with chronic hepatitis B,” PLoS ONE, vol. 8, no. 3, Article ID e58236, 2013. View at Publisher · View at Google Scholar · View at Scopus
  5. E. M. Sokal, M. Paganelli, S. Wirth et al., “Management of chronic hepatitis B in childhood: ESPGHAN clinical practice guidelines: consensus of an expert panel on behalf of the European Society of Pediatric Gastroenterology, Hepatology and Nutrition,” Journal of Hepatology, vol. 59, no. 4, pp. 814–829, 2013. View at Publisher · View at Google Scholar · View at Scopus
  6. F. Bortolotti, M. Guido, S. Bartolacci et al., “Chronic hepatitis B in children after e antigen seroclearance: final report of a 29-year longitudinal study,” Hepatology, vol. 43, no. 3, pp. 556–562, 2006. View at Publisher · View at Google Scholar · View at Scopus
  7. R. Iorio, A. Giannattasio, F. Cirillo, L. D'Alessandro, and A. Vegnente, “Long-term outcome in children with chronic hepatitis B: a 24-year observation period,” Clinical Infectious Diseases, vol. 45, no. 8, pp. 943–949, 2007. View at Publisher · View at Google Scholar · View at Scopus
  8. Y.-H. Ni, M.-H. Chang, P.-J. Chen et al., “Viremia profiles in children with chronic hepatitis B virus infection and spontaneous e antigen seroconversion,” Gastroenterology, vol. 132, no. 7, pp. 2340–2345, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. Y. Chen, A. Shen, P. J. Rider et al., “A liver-specific microRNA binds to a highly conserved RNA sequence of hepatitis B virus and negatively regulates viral gene expression and replication,” The FASEB Journal, vol. 25, no. 12, pp. 4511–4521, 2011. View at Publisher · View at Google Scholar · View at Scopus
  10. R. M. O'Connell, D. S. Rao, A. A. Chaudhuri, and D. Baltimore, “Physiological and pathological roles for microRNAs in the immune system,” Nature Reviews Immunology, vol. 10, no. 2, pp. 111–122, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Esteller, “Non-coding RNAs in human disease,” Nature Reviews Genetics, vol. 12, no. 12, pp. 861–874, 2011. View at Publisher · View at Google Scholar · View at Scopus
  12. Statens Serum Institut (SSI), Mandatory Notification Systems, SSI, Copenhagen, Denmark, 2013, http://www.ssi.dk/English/HealthdataandICT/Surveillance%20in%20Denmark/Mandatory%20notification%20systems.aspx.
  13. “EASL clinical practice guidelines: management of chronic hepatitis B virus infection,” Journal of Hepatology, vol. 57, no. 1, pp. 167–185, 2012.
  14. B. A. Haber, J. M. Block, M. M. Jonas et al., “Recommendations for screening, monitoring, and referral of pediatric chronic hepatitis B,” Pediatrics, vol. 124, no. 5, pp. e1007–e1013, 2009. View at Publisher · View at Google Scholar · View at Scopus
  15. A. S. F. Lok and B. J. McMahon, “Chronic hepatitis B: update of recommendations,” Hepatology, vol. 39, no. 3, pp. 857–861, 2004. View at Publisher · View at Google Scholar · View at Scopus
  16. K. J. Livak and T. D. Schmittgen, “Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method,” Methods, vol. 25, no. 4, pp. 402–408, 2001. View at Publisher · View at Google Scholar · View at Scopus
  17. J.-H. Yang, J.-H. Li, P. Shao, H. Zhou, Y.-Q. Chen, and L.-H. Qu, “StarBase: a database for exploring microRNA-mRNA interaction maps from Argonaute CLIP-Seq and Degradome-Seq data,” Nucleic Acids Research, vol. 39, no. 1, pp. D202–D209, 2011. View at Publisher · View at Google Scholar · View at Scopus
  18. X. Liu, X. Yu, D. J. Zack, H. Zhu, and J. Qian, “TiGER: a database for tissue-specific gene expression and regulation,” BMC Bioinformatics, vol. 9, article 271, 2008. View at Publisher · View at Google Scholar · View at Scopus
  19. S.-J. Xiao, C. Zhang, Q. Zou, and Z.-L. Ji, “TiSGeD: a database for tissue-specific genes,” Bioinformatics, vol. 26, no. 9, Article ID btq109, pp. 1273–1275, 2010. View at Publisher · View at Google Scholar · View at Scopus
  20. T. N. Winther, I. L. Heiberg, C. H. Bang-Berthelsen, F. Pociot, and B. Hogh, “Hepatitis B surface antigen quantity positively correlates with plasma levels of microRNAs differentially expressed in immunological phases of chronic hepatitis B in children,” PLoS ONE, vol. 8, no. 11, Article ID e80384, 2013. View at Publisher · View at Google Scholar · View at Scopus
  21. H.-T. Zhu, Q.-Z. Dong, G. Wang et al., “Identification of suitable reference genes for qRT-PCR analysis of circulating microRNAs in hepatitis B virus-infected patients,” Molecular Biotechnology, vol. 50, no. 1, pp. 49–56, 2012. View at Publisher · View at Google Scholar · View at Scopus
  22. J. Vandesompele, K. De Preter, F. Pattyn et al., “Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes,” Genome Biology, vol. 3, no. 7, 2002. View at Google Scholar · View at Scopus
  23. G. Amaddeo, C. Guichard, S. Imbeaud, and J. Zucman-Rossi, “Next-generation sequencing identified new oncogenes and tumor suppressor genes in human hepatic tumors,” OncoImmunology, vol. 1, no. 9, pp. 1612–1613, 2012. View at Publisher · View at Google Scholar · View at Scopus
  24. J. Huang, Q. Deng, Q. Wang et al., “Exome sequencing of hepatitis B virus-associated hepatocellular carcinoma,” Nature Genetics, vol. 44, no. 10, pp. 1117–1121, 2012. View at Google Scholar
  25. T. Saitoh, J. Moriwaki, J. Koike et al., “Molecular cloning and characterization of FRAT2, encoding a positive regulator of the WNT signaling pathway,” Biochemical and Biophysical Research Communications, vol. 281, no. 3, pp. 815–820, 2001. View at Publisher · View at Google Scholar · View at Scopus
  26. J. Dudas, T. Mansuroglu, F. Moriconi et al., “Altered regulation of Prox1-gene-expression in liver tumors,” BMC Cancer, vol. 8, article 92, 2008. View at Publisher · View at Google Scholar · View at Scopus
  27. Q. Feng, J. E. Stern, S. E. Hawes, H. Lu, M. Jiang, and N. B. Kiviat, “DNA methylation changes in normal liver tissues and hepatocellular carcinoma with different viral infection,” Experimental and Molecular Pathology, vol. 88, no. 2, pp. 287–292, 2010. View at Publisher · View at Google Scholar · View at Scopus
  28. N. Trehanpati, S. Shrivastav, B. Shivakumar et al., “Analysis of Notch and TGF-β signaling expression in different stages of disease progression during hepatitis B virus infection,” Clinical and Translational Gastroenterology, vol. 3, article e23, 2012. View at Publisher · View at Google Scholar · View at Scopus
  29. L. Yao, F.-J. Li, Z.-Q. Tang, S. Gao, and D.-Q. Wu, “Smad4 expression in hepatocellular carcinoma differs by hepatitis status,” Asian Pacific Journal of Cancer Prevention, vol. 13, no. 4, pp. 1297–1303, 2012. View at Publisher · View at Google Scholar · View at Scopus
  30. E. A. Conner, E. R. Lemmer, M. Omori, P. J. Wirth, V. M. Factor, and S. S. Thorgeirsson, “Dual functions of E2F-1 in a transgenic mouse model of liver carcinogenesis,” Oncogene, vol. 19, no. 44, pp. 5054–5062, 2000. View at Publisher · View at Google Scholar · View at Scopus
  31. K. Takahashi, N. Ikeda, N. Nonoguchi et al., “Enhanced expression of coproporphyrinogen oxidase in malignant brain tumors: CPOX expression and 5-ALA-induced fluorescence,” Neuro-Oncology, vol. 13, no. 11, pp. 1234–1243, 2011. View at Publisher · View at Google Scholar · View at Scopus
  32. F. Shen, J. Li, W. Cai et al., “GATA6 predicts prognosis and hepatic metastasis of colorectal cancer,” Oncology Reports, vol. 30, no. 3, pp. 1355–1361, 2013. View at Publisher · View at Google Scholar · View at Scopus
  33. T. Heise, G. Sommer, K. Reumann, I. Meyer, H. Will, and H. Schaal, “The hepatitis B virus PRE contains a splicing regulatory element,” Nucleic Acids Research, vol. 34, no. 1, pp. 353–363, 2006. View at Publisher · View at Google Scholar · View at Scopus
  34. Y.-H. Ou, P.-H. Chung, F.-F. Hsu, T.-P. Sun, W.-Y. Chang, and S.-Y. Shieh, “The candidate tumor suppressor BTG3 is a transcriptional target of p53 that inhibits E2F1,” The EMBO Journal, vol. 26, no. 17, pp. 3968–3980, 2007. View at Publisher · View at Google Scholar · View at Scopus
  35. P. Landgraf, M. Rusu, R. Sheridan et al., “A mammalian microRNA expression atlas based on small RNA library sequencing,” Cell, vol. 129, no. 7, pp. 1401–1414, 2007. View at Publisher · View at Google Scholar · View at Scopus
  36. Z. Li, X. Gu, Y. Fang, J. Xiang, and Z. Chen, “microRNA expression profiles in human colorectal cancers with brain metastases,” Oncology Letters, vol. 3, no. 2, pp. 346–350, 2012. View at Publisher · View at Google Scholar · View at Scopus
  37. H. Xie, L. Lee, S. Caramuta et al., “MicroRNA expression patterns related to merkel cell polyomavirus infection in human Merkel cell carcinoma,” The Journal of Investigative Dermatology, vol. 134, no. 2, pp. 507–517, 2014. View at Publisher · View at Google Scholar · View at Scopus
  38. A. Markou, I. Sourvinou, P. A. Vorkas, G. M. Yousef, and E. Lianidou, “Clinical evaluation of microRNA expression profiling in non small cell lung cancer,” Lung Cancer, vol. 81, no. 3, pp. 388–396, 2013. View at Publisher · View at Google Scholar · View at Scopus
  39. L. Li, Z. Guo, J. Wang, Y. Mao, and Q. Gao, “Serum miR-18a: a potential marker for hepatitis B virus-related hepatocellular carcinoma screening,” Digestive Diseases and Sciences, vol. 57, no. 11, pp. 2910–2916, 2012. View at Publisher · View at Google Scholar · View at Scopus
  40. J. Gui, Y. Tian, X. Wen et al., “Serum microRNA characterization identifies miR-885-5p as a potential marker for detecting liver pathologies,” Clinical Science, vol. 120, no. 5, pp. 183–193, 2011. View at Publisher · View at Google Scholar · View at Scopus
  41. X.-M. Zhu, L.-J. Wu, J. Xu, R. Yang, and F.-S. Wu, “Let-7c MicroRNA expression and clinical significance in hepatocellular carcinoma,” Journal of International Medical Research, vol. 39, no. 6, pp. 2323–2329, 2011. View at Publisher · View at Google Scholar · View at Scopus
  42. H.-Y. Jia, Y.-X. Wang, W.-T. Yan et al., “MicroRNA-125b functions as a tumor suppressor in hepatocellular carcinoma cells,” International Journal of Molecular Sciences, vol. 13, no. 7, pp. 8762–8774, 2012. View at Publisher · View at Google Scholar · View at Scopus
  43. C. Xu, S. Liu, H. Fu et al., “MicroRNA-193b regulates proliferation, migration and invasion in human hepatocellular carcinoma cells,” European Journal of Cancer, vol. 46, no. 15, pp. 2828–2836, 2010. View at Publisher · View at Google Scholar · View at Scopus
  44. S.-M. Kang, H.-J. Lee, and J.-Y. Cho, “MicroRNA-365 regulates NKX2-1, a key mediator of lung cancer,” Cancer Letters, vol. 335, no. 2, pp. 487–494, 2013. View at Publisher · View at Google Scholar · View at Scopus
  45. S. Shimizu, T. Takehara, H. Hikita et al., “The let-7 family of microRNAs inhibits Bcl-xL expression and potentiates sorafenib-induced apoptosis in human hepatocellular carcinoma,” Journal of Hepatology, vol. 52, no. 5, pp. 698–704, 2010. View at Publisher · View at Google Scholar · View at Scopus
  46. L. Zeng, J. Yu, T. Huang et al., “Differential combinatorial regulatory network analysis related to venous metastasis of hepatocellular carcinoma,” BMC Genomics, vol. 13, supplement 8, article S14, 2012. View at Google Scholar · View at Scopus
  47. A. Fujimoto, Y. Totoki, T. Abe et al., “Whole-genome sequencing of liver cancers identifies etiological influences on mutation patterns and recurrent mutations in chromatin regulators,” Nature Genetics, vol. 44, no. 7, pp. 760–764, 2012. View at Publisher · View at Google Scholar · View at Scopus
  48. S. A. Bossone, C. Asselin, A. J. Patel, and K. B. Marcu, “MAZ, a zinc finger protein, binds to c-MYC and C2 gene sequences regulating transcriptional initiation and termination,” Proceedings of the National Academy of Sciences of the United States of America, vol. 89, no. 16, pp. 7452–7456, 1992. View at Publisher · View at Google Scholar · View at Scopus
  49. N. G. Nagl Jr., D. R. Zweitzig, B. Thimmapaya, G. R. Beck Jr., and E. Moran, “The c-myc gene is a direct target of mammalian SWI/SNF-related complexes during differentiation-associated cell cycle arrest,” Cancer Research, vol. 66, no. 3, pp. 1289–1293, 2006. View at Publisher · View at Google Scholar · View at Scopus
  50. M. Bechard, R. Trost, A. M. Singh, and S. Dalton, “Frat is a phosphatidylinositol 3-kinase/akt-regulated determinant of glycogen synthase kinase 3β subcellular localization in pluripotent cells,” Molecular and Cellular Biology, vol. 32, no. 2, pp. 288–296, 2012. View at Publisher · View at Google Scholar · View at Scopus
  51. C. Coulouarn, L. E. Gomez-Quiroz, J.-S. Lee et al., “Oncogene-specific gene expression signatures at preneoplastic stage in mice define distinct mechanisms of hepatocarcinogenesis,” Hepatology, vol. 44, no. 4, pp. 1003–1011, 2006. View at Publisher · View at Google Scholar · View at Scopus
  52. L. Song, H. Liu, S. Gao, W. Jiang, and W. Huang, “Cellular microRNAs inhibit replication of the H1N1 influenza A virus in infected cells,” Journal of Virology, vol. 84, no. 17, pp. 8849–8860, 2010. View at Publisher · View at Google Scholar · View at Scopus
  53. A. Formosa, E. K. Markert, A. M. Lena et al., “MicroRNAs, miR-154, miR-299-5p, miR-376a, miR-376c, miR-377, miR-381, miR-487b, miR-485-3p, miR-495 and miR-654-3p, mapped to the 14q32.31 locus, regulate proliferation, apoptosis, migration and invasion in metastatic prostate cancer cells,” Oncogene, vol. 33, pp. 5173–5182, 2014. View at Publisher · View at Google Scholar · View at Scopus
  54. S. Taketani, T. Furukawa, and K. Furuyama, “Expression of coproporphyrinogen oxidase and synthesis of hemoglobin in human erythroleukemia K562 cells,” European Journal of Biochemistry/FEBS, vol. 268, no. 6, pp. 1705–1711, 2001. View at Publisher · View at Google Scholar · View at Scopus
  55. M. Corioni, N. Antih, G. Tanackovic, M. Zavolan, and A. Krämer, “Analysis of in situ pre-mRNA targets of human splicing factor SF1 reveals a function in alternative splicing,” Nucleic Acids Research, vol. 39, no. 5, pp. 1868–1879, 2011. View at Publisher · View at Google Scholar · View at Scopus
  56. H. L. Janssen, H. W. Reesink, E. J. Lawitz et al., “Treatment of HCV infection by targeting microRNA,” The New England Journal of Medicine, vol. 368, no. 18, pp. 1685–1694, 2013. View at Publisher · View at Google Scholar · View at Scopus