Aflatoxin B1 induces persistent epigenomic effects in primary human hepatocytes associated with hepatocellular carcinoma

Toxicology

Volumn 350-352, Issue , 2016, Pages 31-39

  Rieswijk, Linda ^a,b   Claessen, Sandra M H ^a   Bekers, Otto ^c   van Herwijnen, Marcel ^a   Theunissen, Daniël H J ^a   Jennen, Danyel G J ^a,b   de Kok, Theo M C M ^a   Kleinjans, Jos C S ^a,b   van Breda, Simone G J ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b Netherlands Toxicogenomics Centre   (Netherlands)

^c MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Aflatoxin B1; Epigenomics; Hepatocellular carcinoma; Persistence; Wash out

Indexed keywords

AFLATOXIN B1; GENOMIC DNA; TRANSCRIPTOME; CARCINOGEN; MESSENGER RNA;

ARTICLE; DNA FOOTPRINTING; DNA METHYLATION; DNA MRNA INTERACTION; ENVIRONMENTAL EXPOSURE; EPIGENETICS; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; LIVER CARCINOGENESIS; LIVER CELL; LIVER CELL CARCINOMA; PRIORITY JOURNAL; RNA BINDING; TRANSCRIPTOMICS; CARCINOGENESIS; CHEMICALLY INDUCED; DNA MICROARRAY; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENETIC EPIGENESIS; GENETICS; LIVER TUMOR; METABOLISM; PATHOLOGY; TIME FACTOR;

AFLATOXIN B1; CARCINOGENESIS; CARCINOGENS; CARCINOMA, HEPATOCELLULAR; DNA METHYLATION; EPIGENESIS, GENETIC; EPIGENOMICS; GENE EXPRESSION PROFILING; HEPATOCYTES; HUMANS; LIVER NEOPLASMS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RNA, MESSENGER; TIME FACTORS;

EID: 84964940072     PISSN: 0300483X     EISSN: 18793185     Source Type: Journal    
DOI: 10.1016/j.tox.2016.05.002     Document Type: Article

References (63)

1. Agola J.O., Jim P.A., Ward H.H., Basuray S., Wandinger-Ness A. Rab GTPases as regulators of endocytosis, targets of disease and therapeutic opportunities. Clin. Genet. 2011, 80:305-318.
2. Alenzi F.Q., El-Nashar E.M., Al-Ghamdi S.S., Abbas M.Y., Hamad A.M., El-Saeed O.M., Wyse R.K., Lotfy M. Original article: investigation of bcl-2 and PCNA in hepatocellular carcinoma: relation to chronic HCV. J. Egypt Natl. Canc. Inst. 2010, 22:87-94.
3. Blazek D., Kohoutek J., Bartholomeeusen K., Johansen E., Hulinkova P., Luo Z., Cimermancic P., Ule J., Peterlin B.M. The cyclin K/Cdk12 complex maintains genomic stability via regulation of expression of DNA damage response genes. Genes Dev. 2011, 25:2158-2172.
4. Brennwald P. Membrane traffic: the exocyst meets the cell cycle. Curr. Biol. 2013, 23:R838-840.
5. Caiment F., Tsamou M., Jennen D., Kleinjans J. Assessing compound carcinogenicity in vitro using connectivity mapping. Carcinog. Adv. 2013, (Access published August 12). 10.1093/carcin/bgt278.
6. Caiment F., Tsamou M., Jennen D., Kleinjans J. Assessing compound carcinogenicity in vitro using connectivity mapping. Carcinogenesis 2014, 35:201-207.
7. Coonen M., Theunissen D.H., Kleinjans J.C., Jennen D.G. MagiCMicroRna: a web implementation of AgiMicroRna using shiny. Source Code Biol. Med. 2015, 10:4.
8. Davis A.P., Murphy C.G., Johnson R., Lay J.M., Lennon-Hopkins K., Saraceni-Richards C., Sciaky D., King B.L., Rosenstein M.C., Wiegers T.C., Mattingly C.J. The comparative toxicogenomics database: update 2013. Nucleic Acids Res. 2013, 41:D1104-1114.
9. Dong W.W., Mou Q., Chen J., Cui J.T., Li W.M., Xiao W.H. Differential expression of Rab27A/B correlates with clinical outcome in hepatocellular carcinoma. World J. Gastroenterol. 2012, 18:1806-1813.
10. Edgar R., Domrachev M., Lash A.E. Gene expression omnibus: nCBI gene expression and hybridization array data repository. Nucleic Acids Res. 2002, 30:207-210.
11. Edwards M.C., Liegeois N., Horecka J., DePinho R.A., Sprague G.F., Tyers M., Elledge S.J. Human CPR (cell cycle progression restoration) genes impart a Far-phenotype on yeast cells. Genetics 1997, 147:1063-1076.
12. Edwards M.C., Wong C., Elledge S.J. Human cyclin K, a novel RNA polymerase II-associated cyclin possessing both carboxy-terminal domain kinase and Cdk-activating kinase activity. Mol. Cell. Biol. 1998, 18:4291-4300.
13. Eijssen L.M., Jaillard M., Adriaens M.E., Gaj S., de Groot P.J., Muller M., Evelo C.T. User-friendly solutions for microarray quality control and pre-processing on ArrayAnalysis.org. Nucleic Acids Res. 2013, 41:W71-76.
14. Espinosa J.M. Histone H2B ubiquitination: the cancer connection. Genes Dev. 2008, 22:2743-2749.
15. Fornari F., Gramantieri L., Ferracin M., Veronese A., Sabbioni S., Calin G.A., Grazi G.L., Giovannini C., Croce C.M., Bolondi L., Negrini M. MiR-221 controls CDKN1C/p57 and CDKN1B/p27 expression in human hepatocellular carcinoma. Oncogene 2008, 27:5651-5661.
16. Fornari F., Gramantieri L., Giovannini C., Veronese A., Ferracin M., Sabbioni S., Calin G.A., Grazi G.L., Croce C.M., Tavolari S., Chieco P., Negrini M., Bolondi L. MiR-122/cyclin G1 interaction modulates p53 activity and affects doxorubicin sensitivity of human hepatocarcinoma cells. Cancer Res. 2009, 69:5761-5767.
17. Fu T.J., Peng J., Lee G., Price D.H., Flores O. Cyclin K functions as a CDK9 regulatory subunit and participates in RNA polymerase II transcription. J. Biol. Chem. 1999, 274:34527-34530.
18. Gautier L., Cope L., Bolstad B.M., Irizarry R.A. Affy-analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 2004, 20:307-315.
19. Gentleman R.C., Carey V.J., Bates D.M., Bolstad B., Dettling M., Dudoit S., Ellis B., Gautier L., Ge Y., Gentry J., Hornik K., Hothorn T., Huber W., Iacus S., Irizarry R., Leisch F., Li C., Maechler M., Rossini A.J., Sawitzki G., Smith C., Smyth G., Tierney L., Yang J.Y., Zhang J. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 2004, 5:R80.
20. Goodman J.I., Augustine K.A., Cunnningham M.L., Dixon D., Dragan Y.P., Falls J.G., Rasoulpour R.J., Sills R.C., Storer R.D., Wolf D.C., Pettit S.D. What do we need to know prior to thinking about incorporating an epigenetic evaluation into safety assessments?. Toxicol. Sci. 2010, 116:375-381.
21. Gramantieri L., Fornari F., Callegari E., Sabbioni S., Lanza G., Croce C.M., Bolondi L., Negrini M. MicroRNA involvement in hepatocellular carcinoma. J. Cell. Mol. Med. 2008, 12:2189-2204.
22. Groopman J.D., Kensler T.W., Wild C.P. Protective interventions to prevent aflatoxin-induced carcinogenesis in developing countries. Annu. Rev. Public Health 2008, 29:187-203.
23. Hartl D.L., Freifelder D., Snyder L.A. Basic Genetics 1988, Jones and Bartlett Publishers, Boston.
24. Hou L., Zhang X., Wang D., Baccarelli A. Environmental chemical exposures and human epigenetics. Int. J. Epidemiol. 2012, 41:79-105.
25. Hsu I.C., Metcalf R.A., Sun T., Welsh J.A., Wang N.J., Harris C.C. Mutational hotspot in the p53 gene in human hepatocellular carcinomas. Nature 1991, 350:427-428.
26. Hu T.H., Wang C.C., Huang C.C., Chen C.L., Hung C.H., Chen C.H., Wang J.H., Lu S.N., Lee C.M., Changchien C.S., Tai M.H. Down-regulation of tumor suppressor gene PTEN, overexpression of p53, plus high proliferating cell nuclear antigen index predict poor patient outcome of hepatocellular carcinoma after resection. Oncol. Rep. 2007, 18:1417-1426.
27. Hussain S.P., Schwank J., Staib F., Wang X.W., Harris C.C. TP53 mutations and hepatocellular carcinoma: insights into the etiology and pathogenesis of liver cancer. Oncogene 2007, 26:2166-2176.
28. Izzotti A., Pulliero A. The effects of environmental chemical carcinogens on the microRNA machinery. Int. J. Hyg. Environ. Health 2014, 217:601-627.
29. Kamburov A., Wierling C., Lehrach H., Herwig R. ConsensusPathDB-a database for integrating human functional interaction networks. Nucleic Acids Res. 2009, 37:D623-628.
30. Karakatsanis A., Papaconstantinou I., Gazouli M., Lyberopoulou A., Polymeneas G., Voros D. Expression of microRNAs, miR-21, miR-31, miR-122, miR-145, miR-146a, miR-200c, miR-221, miR-222, and miR-223 in patients with hepatocellular carcinoma or intrahepatic cholangiocarcinoma and its prognostic significance. Mol. Carcinog. 2013, 52:297-303.
31. Koufaris C., Wright J., Currie R.A., Gooderham N.J. Hepatic microRNA profiles offer predictive and mechanistic insights after exposure to genotoxic and epigenetic hepatocarcinogens. Toxicol. Sci. 2012, 128:532-543.
32. Lai H., Mo X., Yang Y., He K., Xiao J., Liu C., Chen J., Lin Y. Association between aflatoxin B1 occupational airway exposure and risk of hepatocellular carcinoma: a case-control study. Tumour Biol. 2014, 35:9577-9584.
33. Legler J. Epigenetics: an emerging field in environmental toxicology. Integr. Environ. Assess. Manage. 2010, 6:314-315.
34. Liu Y., Wu F. Global burden of aflatoxin-induced hepatocellular carcinoma: a risk assessment. Environ. Health Perspect. 2010, 118:818-824.
35. Lopez-Romero P. Pre-processing and differential expression analysis of Agilent microRNA arrays using the AgiMicroRna Bioconductor library. BMC Genomics 2011, 12:64.
36. Marsaud V., Tchakarska G., Andrieux G., Liu J.M., Dembele D., Jost B., Wdzieczak-Bakala J., Renoir J.M., Sola B. Cyclin K and cyclin D1b are oncogenic in myeloma cells. Mol. Cancer 2010, 9:103.
37. McLeod R., Ellis E.M., Arthur J.R., Neal G.E., Judah D.J., Manson M.M., Hayes J.D. Protection conferred by selenium deficiency against aflatoxin B1 in the rat is associated with the hepatic expression of an aldo-keto reductase and a glutathione S-transferase subunit that metabolize the mycotoxin. Cancer Res. 1997, 57:4257-4266.
38. Mirbahai L., Chipman J.K. Epigenetic memory of environmental organisms: a reflection of lifetime stressor exposures. Mutat. Res. Genet. Toxicol. Environ. Mutagen. 2014, 764-765:10-17.
39. Moggs J.G., Goodman J.I., Trosko J.E., Roberts R.A. Epigenetics and cancer: implications for drug discovery and safety assessment. Toxicol. Appl. Pharmacol. 2004, 196:422-430.
40. Moldovan G.L., Pfander B., Jentsch S. PCNA, the maestro of the replication fork. Cell 2007, 129:665-679.
41. Morgan M.J., Liu Z.-g. Crosstalk of reactive oxygen species and NF-κB signaling. Cell Res. 2011, 21:103-115.
42. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 1983, 65:55-63.
43. Nürnberg A., Kitzing T., Grosse R. Nucleating actin for invasion. Nat. Rev. Cancer 2011, 11:177-187.
44. Nayak S.R., Harrington E., Boone D., Hartmaier R., Chen J., Pathiraja T.N., Cooper K.L., Fine J.L., Sanfilippo J., Davidson N.E., Lee A.V., Dabbs D., Oesterreich S. A role for histone H2B variants in endocrine-resistant breast cancer. Horm'. Cancer 2015, 6(5-6):214-224.
45. Qian G., Tang L., Wang F., Guo X., Massey M.E., Williams J.H., Phillips T.D., Wang J.S. Physiologically based toxicokinetics of serum aflatoxin B1-lysine adduct in F344 rats. Toxicology 2013, 303:147-151.
46. Qin L.F., Ng I.O., Fan S.T., Ng M. p21/WAF1, p53 and PCNA expression and p53 mutation status in hepatocellular carcinoma. Int. J. Cancer 1998, 79:424-428.
47. Rebhan M., Chalifa-Caspi V., Prilusky J., Lancet D. GeneCards: integrating information about genes, proteins and diseases. Trends Genet. 1997, 13:163.
48. Rieswijk L., Lizarraga D., Brauers K.J., Kleinjans J.C., van Delft J.H. Characterisation of cisplatin-induced transcriptomics responses in primary mouse hepatocytes, HepG2 cells and mouse embryonic stem cells shows conservation of regulating transcription factor networks. Mutagenesis 2014, 29:17-26.
49. Saitoh M., Nishitoh H., Fujii M., Takeda K., Tobiume K., Sawada Y., Kawabata M., Miyazono K., Ichijo H. Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. EMBO J. 1998, 17:2596-2606.
50. Smyth G.K. Limma: Linear Models for Microarray Data 2005, Springer, New York.
51. Soini Y., Chia S.C., Bennett W.P., Groopman J.D., Wang J.S., DeBenedetti V.M., Cawley H., Welsh J.A., Hansen C., Bergasa N.V., Jones E.A., DiBisceglie A.M., Trivers G.E., Sandoval C.A., Calderon I.E., Munoz Espinosa L.E., Harris C.C. An aflatoxin-associated mutational hotspot at codon 249 in the p53 tumor suppressor gene occurs in hepatocellular carcinomas from Mexico. Carcinogenesis 1996, 17:1007-1012.
52. Subramani D., Alahari S.K. Integrin-mediated function of Rab GTPases in cancer progression. Mol. Cancer 2010, 9:312.
53. Sun J., Lu H., Wang X., Jin H. MicroRNAs in hepatocellular carcinoma: regulation, function, and clinical implications. Sci. World J. 2013, 2013:924206.
54. Valinluck V., Tsai H.H., Rogstad D.K., Burdzy A., Bird A., Sowers L.C. Oxidative damage to methyl-CpG sequences inhibits the binding of the methyl-CpG binding domain (MBD) of methyl-CpG binding protein 2 (MeCP2). Nucleic Acids Res. 2004, 32:4100-4108.
55. van Breda S.G., Claessen S.M., Lo K., van Herwijnen M., Brauers K.J., Lisanti S., Theunissen D.H., Jennen D.G., Gaj S., de Kok T.M., Kleinjans J.C. Epigenetic mechanisms underlying arsenic-associated lung carcinogenesis. Arch. Toxicol. 2015, 89:1959-1969.
56. Wennerberg K., Rossman K.L., Der C.J. The Ras superfamily at a glance. J. Cell Sci. 2005, 118:843-846.
57. Wild C.P., Gong Y.Y. Mycotoxins and human disease: a largely ignored global health issue. Carcinogenesis 2010, 31:71-82.
58. Yasui D.H., Peddada S., Bieda M.C., Vallero R.O., Hogart A., Nagarajan R.P., Thatcher K.N., Farnham P.J., Lasalle J.M. Integrated epigenomic analyses of neuronal MeCP2 reveal a role for long-range interaction with active genes. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:19416-19421.
59. Young M.D., Willson T.A., Wakefield M.J., Trounson E., Hilton D.J., Blewitt M.E., Oshlack A., Majewski I.J. ChIP-seq analysis reveals distinct H3K27me3 profiles that correlate with transcriptional activity. Nucleic Acids Res. 2011, 39:7415-7427.
60. Zhang Y.J., Ahsan H., Chen Y., Lunn R.M., Wang L.Y., Chen S.Y., Lee P.H., Chen C.J., Santella R.M. High frequency of promoter hypermethylation of RASSF1A and p16 and its relationship to aflatoxin B1-DNA adduct levels in human hepatocellular carcinoma. Mol. Carcinog. 2002, 35:85-92.
61. Zhang Y.J., Chen Y., Ahsan H., Lunn R.M., Lee P.H., Chen C.J., Santella R.M. Inactivation of the DNA repair gene O6-methylguanine-DNA methyltransferase by promoter hypermethylation and its relationship to aflatoxin B1-DNA adducts and p53 mutation in hepatocellular carcinoma. Int. J. Cancer 2003, 103:440-444.
62. Zhang Y.J., Rossner P., Chen Y., Agrawal M., Wang Q., Wang L., Ahsan H., Yu M.W., Lee P.H., Santella R.M. Aflatoxin B1 and polycyclic aromatic hydrocarbon adducts, p53 mutations and p16 methylation in liver tissue and plasma of hepatocellular carcinoma patients. Int. J. Cancer 2006, 119:985-991.
63. Zhang Y.J., Wu H.C., Yazici H., Yu M.W., Lee P.H., Santella R.M. Global hypomethylation in hepatocellular carcinoma and its relationship to aflatoxin B(1) exposure. World J. Hepatol. 2012, 4:169-175.