Trans-nonachlor decreases miR-141-3p levels in human melanocytes in vitro promoting melanoma cell characteristics and shows a multigenerational impact on miR-8 levels in Drosophila

Toxicology

Volumn 368-369, Issue , 2016, Pages 129-141

  Verrando, Patrick ^a   Capovilla, Maria ^b   Rahmani, Roger ^a  

^a TOXALIM RESEARCH CENTRE IN FOOD TOXICOLOGY   (France)

^b Institut Sophia Agrobiotech   (France)

Author keywords

Drosophila; Melanoma; miR 141 3 p; miR 8; Trans nonachlor; Vasculogenic mimicry

Indexed keywords

4 IODO 2,5 DIMETHOXYAMPHETAMINE; ENDOCRINE DISRUPTOR; MICRORNA; MICRORNA 141 3P; MICRORNA 8; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; NONACHLOR; PHOSPHATIDYLINOSITOL 3 KINASE; TRANS NONACHLOR; UNCLASSIFIED DRUG; VASCULAR ENDOTHELIAL CADHERIN; CADHERIN; CHLORINATED HYDROCARBON; INSECTICIDE; LEUKOCYTE ANTIGEN; MIR-8 MICRORNA, DROSOPHILA; MIRN141 MICRORNA, HUMAN;

ANCHORAGE INDEPENDENT GROWTH; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; FEMALE; GENE EXPRESSION; GROWTH INHIBITION; HUMAN; HUMAN CELL; IN VITRO STUDY; MALE; MELANOCYTE; MELANOMA; MELANOMA CELL LINE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; ANIMAL; CHEMICALLY INDUCED; DISEASE MODEL; DROSOPHILA; DRUG EFFECTS; GENETIC EPIGENESIS; GENETIC TRANSFECTION; GENETICS; METABOLISM; TUMOR CELL LINE;

ANIMALS; ANTIGENS, CD; CADHERINS; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; DOWN-REGULATION; DROSOPHILA; EPIGENESIS, GENETIC; HUMANS; HYDROCARBONS, CHLORINATED; INSECTICIDES; MELANOCYTES; MELANOMA; MICRORNAS; MITOGEN-ACTIVATED PROTEIN KINASE 3; PHOSPHATIDYLINOSITOL 3-KINASES; TRANSFECTION;

EID: 84988424184     PISSN: 0300483X     EISSN: 18793185     Source Type: Journal    
DOI: 10.1016/j.tox.2016.09.003     Document Type: Article

References (62)

1. Abbott, D.E., Bailey, C.M., Postovit, L.-M., Seftor, E.A., Margaryan, N., Seftor, R.E.B., Hendrix, M.J.C., The epigenetic influence of tumor and embryonic microenvironments: how different are they?. Cancer Microenviron. 1 (2008), 13–21, 10.1007/s12307-008-0004-5.
2. Alavanja, M.C., Sandler, D.P., McMaster, S.B., Zahm, S.H., McDonnell, C.J., Lynch, C.F., Pennybacker, M., Rothman, N., Dosemeci, M., Bond, A.E., Blair, A., The agricultural health study. Environ. Health Perspect. 104 (1996), 362–369.
3. Bennett, G.W., Ballee, D.L., Hall, R.C., Fahey, J.E., Butts, W.L., Osmun, J.V., Persistence and distribution of chlordane and dieldrin applied as termiticides. Bull. Environ. Contam. Toxicol. 11 (1974), 64–69.
4. Bondy, G.S., Newsome, W.H., Armstrong, C.L., Suzuki, C.A., Doucet, J., Fernie, S., Hierlihy, S.L., Feeley, M.M., Barker, M.G., trans-Nonachlor and cis-nonachlor toxicity in Sprague-Dawley rats: comparison with technical chlordane. Toxicol Sci. 58:2 (2000), 386–398.
5. Cao, Z., Bao, M., Miele, L., Sarkar, F.H., Wang, Z., Zhou, Q., Tumour vasculogenic mimicry is associated with poor prognosis of human cancer patients: a systemic review and meta-analysis. Eur. J. Cancer 49 (2013), 3914–3923, 10.1016/j.ejca.2013.07.148.
6. Casati, L., Sendra, R., Sibilia, V., Celotti, F., Endocrine disrupters: the new players able to affect the epigenome. Front. Cell Dev. Biol., 3, 2015, 37, 10.3389/fcell.2015.00037.
7. Collotta, M., Bertazzi, P.A., Bollati, V., Epigenetics and pesticides. Toxicology 307 (2013), 35–41, 10.1016/j.tox.2013.01.017.
8. Conde-Perez, A., Larue, L., PTEN and melanomagenesis. Future Oncol. 8 (2012), 1109–1120, 10.2217/fon.12.106.
9. Croes, K., Colles, A., Koppen, G., Govarts, E., Bruckers, L., Van de Mieroop, E., Nelen, V., Covaci, A., Dirtu, A.C., Thomsen, C., Haug, L.S., Becher, G., Mampaey, M., Schoeters, G., Van Larebeke, N., Baeyens, W., Persistent organic pollutants (POPs) in human milk: a biomonitoring study in rural areas of Flanders (Belgium). Chemosphere 89:8 (2012), 988–994, 10.1016/j.chemosphere.2012.06.058 Epub 2012 Jul 26.
10. Davalos, V., Esteller, M., MicroRNAs and cancer epigenetics: a macrorevolution. Curr. Opin. Oncol. 22 (2010), 35–45, 10.1097/CCO.0b013e328333dcbb.
11. Dearth, M.A., Hites, R.A., Complete analysis of technical chlordane using negative ionisation mass spectrometry. Environ. Sci. Technol. 25 (1991), 245–254.
12. Dennis, L.K., Lynch, C.F., Sandler, D.P., Alavanja, M.C.R., Pesticide use and cutaneous melanoma in pesticide applicators in the agricultural heath study. Environ. Health Perspect. 118 (2010), 812–817, 10.1289/ehp.0901518.
13. Dimitriadou, L., Malarvannan, G., Covaci, A., Iossifidou, E., Tzafettas, J., Zournatzi-Koiou, V., Kalantzi, O.I., Levels and profiles of brominated and chlorinated contaminants in human breast milk from Thessaloniki, Greece. Sci. Total Environ. 539 (2016), 350–358, 10.1016/j.scitotenv.2015.08.137.
14. Dweep, H., Gretz, N., miRWalk2.0: a comprehensive atlas of microRNA-target interactions. Nat. Methods, 12, 2015, 697, 10.1038/nmeth.3485.
15. Edgecomb, R.S., Harth, C.E., Schneiderman a, M., Regulation of feeding behavior in adult Drosophila melanogaster varies with feeding regime and nutritional state. J. Exp. Biol. 197 (1994), 215–235.
16. Elson-Schwab, I., Lorentzen, A., Marshall, C.J., MicroRNA-200 family members differentially regulate morphological plasticity and mode of melanoma cell invasion. PLoS One, 5, 2010, 10.1371/journal.pone.0013176.
17. Fortes, C., Mastroeni, S., Melchi, F., Pilla, M.A., Alotto, M., Antonelli, G., Camaione, D., Bolli, S., Luchetti, E., Pasquini, P., The association between residential pesticide use and cutaneous melanoma. Eur. J. Cancer 43 (2007), 1066–1075, 10.1016/j.ejca.2007.01.013.
18. Foster, W.G., Cheung, A.P., Davis, K., Graves, G., Jarrell, J., Leblanc, A., Liang, C.L., Leech, T., Walker, M., Weber, J.P., Van Oostdam, J., Circulating metals and persistent organic pollutant concentrations in Canadian and non-Canadian born primiparous women from five Canadian centres: results of a pilot biomonitoring study. Sci. Total Environ. 435–436 (2012), 326–336, 10.1016/j.scitotenv.2012.06.070.
19. Gallagher, R.P., Macarthur, A.C., Lee, T.K., Weber, J.-P., Leblanc, A., Mark Elwood, J., Borugian, M., Abanto, Z., Spinelli, J.J., Plasma levels of polychlorinated biphenyls and risk of cutaneous malignant melanoma: a preliminary study. Int. J. Cancer 128 (2011), 1872–1880, 10.1002/ijc.25503.
20. Gandini, S., Autier, P., Boniol, M., Reviews on sun exposure and artificial light and melanoma. Prog. Biophys. Mol. Biol. 107 (2011), 362–366, 10.1016/j.pbiomolbio.2011.09.011.
21. Glud, M., Gniadecki, R., MicroRNAs in the pathogenesis of malignant melanoma. J. Eur. Acad. Dermatol. Venereol. 27 (2013), 142–150, 10.1111/j.1468-3083.2012.04579.x.
22. Gonzalez, C., Drosophila melanogaster: a model and a tool to investigate malignancy and identify new therapeutics. Nat. Rev. Cancer 13 (2013), 172–183, 10.1038/nrc3461.
23. Hyun, S., Lee, J.H., Jin, H., Nam, J., Namkoong, B., Lee, G., Chung, J., Kim, V.N., Conserved microRNA miR-8/miR-200 and its target USH/FOG2 control growth by regulating PI3K. Cell 139 (2009), 1096–1108, 10.1016/j.cell.2009.11.020.
24. Itzhaki, O., Greenberg, E., Shalmon, B., Kubi, A., Treves, A.J., Shapira-Frommer, R., Avivi, C., Ortenberg, R., Ben-Ami, E., Schachter, J., Besser, M.J., Markel, G., Nicotinamide inhibits vasculogenic mimicry, an alternative vascularization pathway observed in highly aggressive melanoma. PLoS One, 8, 2013, 10.1371/journal.pone.0057160.
25. Ji, J., Qin, Y., Ren, J., Lu, C., Wang, R., Dai, X., Zhou, R., Huang, Z., Xu, M., Chen, M., Wu, W., Song, L., Shen, H., Hu, Z., Miao, D., Xia, Y., Wang, X., Mitochondria-related miR-141-3p contributes to mitochondrial dysfunction in HFD-induced obesity by inhibiting PTEN. Sci. Rep., 5, 2015, 16262, 10.1038/srep16262.
26. Jiang, Q., Wang, Y., Hao, Y., Juan, L., Teng, M., Zhang, X., Li, M., Wang, G., Liu, Y., miR2Disease: a manually curated database for microRNA deregulation in human disease. Nucleic Acids Res. 37 (2009), D98–104, 10.1093/nar/gkn714.
27. Kirschmann, D.A., Seftor, E.A., Hardy, K.M., Seftor, R.E.B., Hendrix, M.J.C., Molecular pathways: vasculogenic mimicry in tumor cells: diagnostic and therapeutic implications. Clin. Cancer Res. 18 (2012), 2726–2732, 10.1158/1078-0432.CCR-11-3237.
28. Leibowitz-Amit, R., Sidi, Y., Avni, D., Aberrations in the micro-RNA biogenesis machinery and the emerging roles of micro-RNAs in the pathogenesis of cutaneous malignant melanoma. Pigment Cell Melanoma Res. 25 (2012), 740–757, 10.1111/pcmr.12018.
29. Lin, L., Liang, H., Wang, Y., Yin, X., Hu, Y., Huang, J., Ren, T., Xu, H., Zheng, L., Chen, X., microRNA-141 inhibits cell proliferation and invasion and promotes apoptosis by targeting hepatocyte nuclear factor-3β in hepatocellular carcinoma cells. BMC Cancer, 14, 2014, 879, 10.1186/1471-2407-14-879.
30. Lissitzky, J.C., Parriaux, D., Ristorcelli, E., Vérine, A., Lombardo, D., Verrando, P., Cyclic AMP signaling as a mediator of vasculogenic mimicry in aggressive human melanoma cells in vitro. Cancer Res. 69 (2009), 802–809, 10.1158/0008-5472.CAN-08-2391.
31. Liu, Y., Ding, Y., Huang, J., Wang, S., Ni, W., Guan, J., Li, Q., Zhang, Y., Ding, Y., Chen, B., Chen, L., MiR-141 suppresses the migration and invasion of HCC cells by targeting Tiam1. PLoS One 9 (2014), 1–10, 10.1371/journal.pone.0088393.
32. Manikkam, M., Haque, M.M., Guerrero-Bosagna, C., Nilsson, E.E., Skinner, M.K., Pesticide methoxychlor promotes the epigenetic transgenerational inheritance of adult-onset disease through the female germline. PLoS One, 9, 2014, 10.1371/journal.pone.0102091.
33. Poell, J.B., van Haastert, R.J., de Gunst, T., Schultz, I.J., Gommans, W.M., Verheul, M., Cerisoli, F., van Noort, P.I., Prevost, G.P., Schaapveld, R.Q.J., Cuppen, E., A functional screen identifies specific micrornas capable of inhibiting human melanoma cell viability. PLoS One, 7, 2012, 10.1371/journal.pone.0043569.
34. Qiao, L., Liang, N., Zhang, J., Xie, J., Liu, F., Xu, D., Yu, X., Tian, Y., Advanced research on vasculogenic mimicry in cancer. J. Cell. Mol. Med. 19 (2015), 315–326, 10.1111/jcmm.12496.
35. Qiu, W., Kassem, M., miR-141-3p inhibits human stromal (mesenchymal) stem cell proliferation and differentiation. Biochim. Biophys. Acta 1843 (2014), 2114–2121, 10.1016/j.bbamcr.2014.06.004.
36. Repetto, G., del Peso, A., Zurita, J.L., Neutral red uptake assay for the estimation of cell viability/cytotoxicity. Nat. Protoc. 3 (2008), 1125–1131, 10.1038/nprot.2008.75.
37. Rudrapatna, V.A., Cagan, R.L., Das, T.K., Drosophila cancer models. Dev. Dyn. 241 (2012), 107–118, 10.1002/dvdy.22771.
38. Sarkar, D., Leung, E.Y., Baguley, B.C., Finlay, G.J., Askarian-Amiri, M.E., Epigenetic regulation in human melanoma: past and future. Epigenetics 2294 (2015), 37–41, 10.1080/15592294.2014.1003746.
39. Segatto, M.M., Bonamigo, R.R., Hohmann, C.B., Muller, K.R., Bakos, L., Mastroeni, S., Fortes, C., Residential and occupational exposure to pesticides may increase risk for cutaneous melanoma: a case-control study conducted in the south of Brazil. Int. J. Dermatol., 2015, 7–11, 10.1111/ijd.12826.
40. Silvy, F., Lissitzky, J.C., Bruneau, N., Zucchini, N., Landrier, J.F., Lombardo, D., Verrando, P., Resistance to cisplatin-induced cell death conferred by the activity of organic anion transporting polypeptides (OATP) in human melanoma cells. Pigment Cell Melanoma Res. 26 (2013), 592–596, 10.1111/pcmr.12108.
41. Skinner, M.K., Endocrine disruptors in 2015: epigenetic transgenerational inheritance. Nat. Rev. Endocrinol. 12 (2015), 2–3, 10.1038/nrendo.2015.206.
42. Slatkin, M., Epigenetic inheritance and the missing heritability problem. Genetics 182 (2009), 845–850, 10.1534/genetics.109.102798.
43. Sloan, C.A., Chan, E.T., Davidson, J.M., Malladi, V.S., Strattan, J.S., Hitz, B.C., Gabdank, I., Narayanan, A.K., Ho, M., Lee, B.T., Rowe, L.D., Dreszer, T.R., Roe, G., Podduturi, N.R., Tanaka, F., Hong, E.L., Cherry, J.M., ENCODE data at the ENCODE portal. Nucleic Acids Res., 44, 2015, 10.1093/nar/gkv1160.
44. Song, Y., Mu, L., Han, X., Li, Q., Dong, B., Li, H., Liu, X., MicroRNA-9 inhibits vasculogenic mimicry of glioma cell lines by suppressing Stathmin expression. J. Neurooncol. 115 (2013), 381–390, 10.1007/s11060-013-1245-9.
45. Stern, S., Snir, O., Mizrachi, E., Galili, M., Zaltsman, I., Soen, Y., Reduction in maternal polycomb levels contributes to transgenerational inheritance of a response to toxic stress in flies. J. Physiol. 592 (2014), 2343–2355, 10.1113/jphysiol.2014.271445.
46. Sun, Q., Zou, X., Zhang, T., Shen, J., Yin, Y., Xiang, J., The role of miR-200a in vasculogenic mimicry and its clinical significance in ovarian cancer. Gynecol. Oncol. 132 (2014), 730–738, 10.1016/j.ygyno.2014.01.047.
47. Trerotola, M., Relli, V., Simeone, P., Alberti, S., Epigenetic inheritance and the missing heritability. Hum. Genomics, 9, 2015, 17, 10.1186/s40246-015-0041-3.
48. Vakonaki, E., Androutsopoulos, V.P., Liesivuori, J., Tsatsakis, A.M., Spandidos, D.A., Pesticides and oncogenic modulation. Toxicology 307 (2013), 42–45, 10.1016/j.tox.2013.01.008.
49. Valery, C., Vasseur, S., Sabatier, F., Iovanna, J.L., Dagorn, J.C., Grob, J.J., Verrando, P., Pancreatitis associated protein I (PAP-I) alters adhesion and motility of human melanocytes and melanoma cells. J. Invest. Dermatol. 116 (2001), 426–433, 10.1046/j.1523-1747.2001.01278.x.
50. Vallejo, D.M., Caparros, E., Dominguez, M., Targeting notch signalling by the conserved miR-8/200 microRNA family in development and cancer cells. EMBO J. 30 (2011), 756–769, 10.1038/emboj.2010.358.
51. VoPham, T., Brooks, M.M., Yuan, J.-M., Talbott, E.O., Ruddell, D., Hart, J.E., Chang, C.-C.H., Weissfeld, J.L., Pesticide exposure and hepatocellular carcinoma risk: a case-control study using a geographic information system (GIS) to link SEER-medicare and California pesticide data. Environ. Res. 143 (2015), 68–82, 10.1016/j.envres.2015.09.027.
52. Vogt, R., Bennett, D., Cassady, D., Frost, J., Ritz, B., Hertz-Picciotto, I., Cancer and non-cancer health effects from food contaminant exposures for children and adults in California: a risk assessment. Environ. Health, 11, 2012, 83, 10.1186/1476-069X-11-83.
53. Waggoner, J.K., Kullman, G.J., Henneberger, P.K., Umbach, D.M., Blair, A., Alavanja, M.C.R., Kamel, F., Lynch, C.F., Knott, C., London, S.J., Hines, C.J., Thomas, K.W., Sandler, D.P., Lubin, J.H., Beane Freeman, L.E., Hoppin, J.A., Mortality in the agricultural health study, 1993–2007. Am. J. Epidemiol. 173 (2011), 71–83, 10.1093/aje/kwq323.
54. Wan, H.Y., Li, Q.Q., Zhang, Y., Tian, W., Li, Y.N., Liu, M., Li, X., Tang, H., MiR-124 represses vasculogenic mimicry and cell motility by targeting amotL1 in cervical cancer cells. Cancer Lett. 355 (2014), 148–158, 10.1016/j.canlet.2014.09.005.
55. Xu, Y., Brenn, T., Brown, E.R.S., Doherty, V., Melton, D.W., Differential expression of microRNAs during melanoma progression: miR-200c, miR-205 and miR-211 are downregulated in melanoma and act as tumour suppressors. Br. J. Cancer 106 (2012), 553–561, 10.1038/bjc.2011.568.
56. Yan, W., Potential roles of noncoding RNAs in environmental epigenetic transgenerational inheritance. Mol. Cell. Endocrinol. 398 (2014), 24–30, 10.1016/j.mce.2014.09.008.
57. Yu, X.Y., Zhang, Z., Liu, J., Zhan, B., Kong, C.Z., MicroRNA-141 is downregulated in human renal cell carcinoma and regulates cell survival by targeting CDC25B. Onco. Targets Ther. 6 (2013), 349–354, 10.2147/OTT.S41343.
58. Yu, K.R., Lee, S., Jung, J.W., Hong, I.S., Kim, H.S., Seo, Y., Shin, T.H., Kang, K.S., MicroRNA-141-3p plays a role in human mesenchymal stem cell aging by directly targeting ZMPSTE24. J. Cell Sci. 126 (2013), 5422–5431, 10.1242/jcs.133314.
59. Zhao, G., Wang, B., Liu, Y., Zhang, J., Deng, S., Qin, Q., Tian, K., Li, X., Zhu, S., Niu, Y., Gong, Q., Wang, C.-Y., miRNA-141, downregulated in pancreatic cancer, inhibits cell proliferation and invasion by directly targeting MAP4K4. Mol. Cancer Ther. 12 (2013), 2569–2580, 10.1158/1535-7163.MCT-13-0296.
60. Zhao, N., Sun, B., Zhao, cun, lan, X., Wang, Y., Sun, H., Dong, zhi, yi, X., Meng, J., Gu, Q., Changes in microRNAs associated with Twist-1 and Bcl-2 overexpression identify signaling pathways. Exp. Mol. Pathol. 99 (2015), 524–532, 10.1016/j.yexmp.2015.08.018.
61. Zhao, X., Wang, Y., Deng, R., Zhang, H., Dou, J., Yuan, H., Hou, G., Du, Y., Chen, Q., Yu, J., miR186 suppresses prostate cancer progression by targeting Twist1. Oncotarget, 2016, 10.18632/oncotarget.8887.
62. van den Hurk, K., Niessen, H.E.C., Veeck, J., van den Oord, J.J., van Steensel, M.A.M., zur Hausen, A., van Engeland, M., Winnepenninckx, V.J.L., Genetics and epigenetics of cutaneous malignant melanoma: a concert out of tune. Biochim. Biophys. Acta – Rev. Cancer 1826 (2012), 89–102, 10.1016/j.bbcan.2012.03.011.