DOI QR코드

DOI QR Code

Aflatoxin B1 Promotes Cell Growth and Invasion in Hepatocellular Carcinoma HepG2 Cells through H19 and E2F1

  • Lv, Jun ;
  • Yu, Ya-Qun ;
  • Li, Shu-Qun ;
  • Luo, Liang ;
  • Wang, Qian
  • Published : 2014.03.30

Abstract

H19 is an imprinted oncofetal gene, and loss of imprinting at the H19 locus results in over-expression of H19 in cancers. Aflatoxin B1(AFB1) is regarded as one of the most dangerous carcinogens. Exposure to AFB1 would most easily increase susceptibility to diseases such as hepatocellular carcinoma(HCC) but any possible relationship between AFB1 and H19 is not clear. In present study, we found that AFB1 could up-regulate the expression of H19 and promote cell growth and invasion by hepatocellular carcinoma HepG2 cells. Knocking down H19 RNA co ld reverse the effects of AFB1 on cell growth and invasion. In addition, AFB1 induced the expression of E2F1 and its knock-down could down-regulate H19 expression and suppress cell growth and invasion in hepatocellular carcinoma HepG2 cells. Furthermore, E2F1 over-expression could up-regulate H19 expression and promote cell growth and invasion, with binding to the H19 promoter being demonstrated by chromatin immunoprecipitation assays (ChIP). In summary, our results suggested that aflatoxin B1could promote cell growth and invasion in hepatocellular carcinoma HepG2 cells through actions on H19 and E2F1.

Keywords

H19;AFB1;cell growth and invasion;hepatocellular carcinoma;E2F1

References

  1. Panzitt K, Tschernatsch MM, Guelly C, et al (2007). Characterization of HULC, a novel gene with striking upregulation in hepatocellular carcinoma, as noncoding RNA. Gastroenterol, 132, 330-42. https://doi.org/10.1053/j.gastro.2006.08.026
  2. McLean M, Dutton MF (1995). Cellular interactions and metabolism of aflatoxin: an update. Pharmacol Ther, 65, 163-92. https://doi.org/10.1016/0163-7258(94)00054-7
  3. Ohtani K (1999). Implication of transcription factor E2F in regulation of DNA replication. Front Biosci, 4, 793-804. https://doi.org/10.2741/Ohtani
  4. Oyagbemi AA, Azeez OI, Saba AB (2010). Hepatocellular carcinoma and the underlying mechanisms. Afr Health Sci, 10, 93-8.
  5. Yang C, Fan J, Zhuang Z, et al (2013). The role of NAD+- dependent isocitrate dehydrogenase 3 subunit $\alpha$ in AFB1 induced liver lesion. Toxicol Lett, 13, 01389-1.
  6. Yang Z, Zhou L, Wu LM, et al (2011). Overexpression of long non-coding RNA HOTAIR predicts tumor recurrence in hepatocellular carcinoma patients following liver transplantation. Ann. Surg. Oncol, 18, 1243-50. https://doi.org/10.1245/s10434-011-1581-y
  7. Zemel S, Bartolomei MS, Tilghman SM (1992). Physical linkage of two mammalian imprinted genes, H19 and insulin-like growth factor 2. Nat Genet, 2, 61-5. https://doi.org/10.1038/ng0992-61
  8. Zhang Y, Tycko B (1992). Monoallelic expression of the human H19 gene. Nat Genet, 1, 40-4. https://doi.org/10.1038/ng0492-40
  9. Zwicker J, Muller R (1997). Cell-cycle regulation of gene expression by transcriptional repression. Trends Genet, 13, 3-6. https://doi.org/10.1016/S0168-9525(96)30112-1
  10. Giannoukakis N, Deal C, Paquette J, et al (1993). Parental genomic imprinting of the human IGF2 gene. Nat Genet, 4, 98-101. https://doi.org/10.1038/ng0593-98
  11. Feng Y, Xue WJ, Li P, et al (2012). RASSF1A hypermethylation is associated with aflatoxin B1 and polycyclic aromatic hydrocarbon exposure in hepatocellular carcinoma. Hepatogastroenterol, 59, 1883-8.
  12. Fry CJ, Pearson A, Malinowski E, et al (1999). Activation of the murine dihydrofolate reductase promoter by E2F1. A requirement for CBP recruitment. J Biol Chem, 274, 15883-91. https://doi.org/10.1074/jbc.274.22.15883
  13. Gabory A, Ripoche MA, Yoshimizu T, et al (2006). The H19 gene: regulation and function of a non-coding RNA. Cytogenet Genome Res, 113, 188-93. https://doi.org/10.1159/000090831
  14. Hanioka N, Nonaka Y, Saito K, et al (2012). Effect of aflatoxin B1 on UDP-glucuronosyltransferase mRNA expression in HepG2 cells. Chemosphere, 89, 526-9. https://doi.org/10.1016/j.chemosphere.2012.05.039
  15. Hibi K, Nakamura H, Hirai A, et al (1996). Loss of H19 imprinting in esophageal cancer. Cancer Res, 56, 480-2.
  16. IARC (2002). Some traditional herbal medicines, some mycotoxins, Naphthalene and Styrene. IARC Press, Lyon.
  17. Khaitan D, Dinger ME, Mazar J, et al (2011). The melanomaupregulated long noncoding RNA SPRY4-IT1 modulates apoptosis and invasion. Cancer Res, 71, 3852-62. https://doi.org/10.1158/0008-5472.CAN-10-4460
  18. Lottin S, Adriaenssens E, Dupressoir T, et al (2002). Overexpression of an ectopic H19 gene enhances the tumorigenic properties of breast cancer cells. Carcinogenesis, 23, 1885-95. https://doi.org/10.1093/carcin/23.11.1885
  19. Luo JH, Ren B, Keryanov S, et al (2006). Transcriptomic and genomic analysis of human hepatocellular carcinomas and hepatoblastomas. Hepatol, 44, 1012-24.
  20. Matouk IJ, DeGroot N, Mezan S, et al (2007). The H19 noncoding RNA is essential for human tumor growth. PLoS One, 2, 845. https://doi.org/10.1371/journal.pone.0000845
  21. Calin GA, Liu CG, Ferracin M, et al (2007). Ultraconserved regions encoding ncRNAs are altered in human leukemias and carcinomas. Cancer Cell, 12, 215-29. https://doi.org/10.1016/j.ccr.2007.07.027
  22. Ayed-Boussema I, Pascussi JM, Maurel P, et al (2012). Effect of aflatoxin B1 on nuclear receptors PXR, CAR, and AhR and their target cytochromes P450 mRNA expression in primary cultures of human hepatocytes. Int J Toxicol, 31, 86-93. https://doi.org/10.1177/1091581811422453
  23. Berteaux N, Lottin S, Monte D, et al (2005). H19 mRNA-like noncoding RNA promotes breast cancer cell proliferation through positive control by E2F1. J Biol Chem, 280, 29625-36. https://doi.org/10.1074/jbc.M504033200
  24. Braconi C, Valeri N, Kogure T, et al (2011). Expression and functional role of a transcribed noncoding RNA with an ultraconserved element in hepatocellular carcinoma. Proc Natl Acad Sci USA, 108, 786-91. https://doi.org/10.1073/pnas.1011098108
  25. Dugimont T, Montpellier C, Adriaenssens E, et al (1998). The H19 TATA-less promoter is efficiently repressed by wild-type tumor suppressor gene product p53. Oncogene, 16, 2395-401. https://doi.org/10.1038/sj.onc.1201742
  26. Dyson N (1994). pRB, p107 and the regulation of the E2F transcription factor. J Cell Sci Suppl, 18, 81-7.
  27. Dyson N (1998). The regulation of E2F by pRB-family proteins. Genes Dev, 12, 2245-62. https://doi.org/10.1101/gad.12.15.2245
  28. Eaton DL, Gallagher EP (1994). Mechanisms of aflatoxin carcinogenesis. Annu Rev Pharmacol, 34, 135-72. https://doi.org/10.1146/annurev.pa.34.040194.001031
  29. Fang Y, Feng Y, Wu T, et al (2013). Aflatoxin B1 negatively regulates Wnt/$\beta$-catenin signaling pathway through activating miR-33a. PLoS One, 8, 73004. https://doi.org/10.1371/journal.pone.0073004
  30. Fellig Y, Ariel I, Ohana P, et al (2005). H19 expression in hepatic metastases from a range of human carcinomas. J Clin Pathol, 58, 1064-8. https://doi.org/10.1136/jcp.2004.023648

Cited by

  1. Functional Roles of Long Non-coding RNA in Human Breast Cancer vol.15, pp.15, 2014, https://doi.org/10.7314/APJCP.2014.15.15.5993
  2. Characteristics of Liver Cancer at Khmer-Soviet Friendship Hospital in Phnom Penh, Cambodia vol.16, pp.1, 2015, https://doi.org/10.7314/APJCP.2015.16.1.35
  3. Long noncoding RNAs in hepatocellular carcinoma: Novel insights into their mechanism vol.7, pp.28, 2015, https://doi.org/10.4254/wjh.v7.i28.2781
  4. Long noncoding RNAs in digestive system cancers: Functional roles, molecular mechanisms, and clinical implications (Review) vol.36, pp.3, 2016, https://doi.org/10.3892/or.2016.4929
  5. Berberine regulates the protein expression of multiple tumorigenesis-related genes in hepatocellular carcinoma cell lines vol.17, pp.1, 2017, https://doi.org/10.1186/s12935-017-0429-3
  6. Long Noncoding RNAs Act as Novel Biomarkers for Hepatocellular Carcinoma: Progress and Prospects vol.2017, pp.2314-6141, 2017, https://doi.org/10.1155/2017/6049480
  7. The Role of Long Non-Coding RNAs in Hepatocarcinogenesis vol.19, pp.3, 2018, https://doi.org/10.3390/ijms19030682
  8. Long non-coding RNA H19 promotes glucose metabolism and cell growth in malignant melanoma via miR-106a-5p/E2F3 axis vol.144, pp.3, 2018, https://doi.org/10.1007/s00432-018-2582-z
  9. Photoinduced discharge of electrons stored in a TiO2-MWCNT composite to an analyte: application to the fluorometric determination of hydrogen peroxide, glucose and aflatoxin B1 vol.185, pp.1, 2018, https://doi.org/10.1007/s00604-017-2583-7
  10. The LncRNA H19/miR-193a-3p axis modifies the radio-resistance and chemotherapeutic tolerance of hepatocellular carcinoma cells by targeting PSEN1 vol.119, pp.10, 2018, https://doi.org/10.1002/jcb.26883
  11. LncRNA H19 overexpression induces bortezomib resistance in multiple myeloma by targeting MCL-1 via miR-29b-3p vol.10, pp.2, 2019, https://doi.org/10.1038/s41419-018-1219-0