The acquisition of cancer stem cell-like properties and neoplastic transformation of human keratinocytes induced by arsenite involves epigenetic silencing of let-7c via Ras/NF-κB

Toxicology Letters

Volumn 227, Issue 2, 2014, Pages 91-98

  Jiang, Rongrong ^a   Li, Yuan ^a   Zhang, Aihua ^b   Wang, Bairu ^a   Xu, Yuan ^a   Xu, Wenchao ^a   Zhao, Yue ^a   Luo, Fei ^a   Liu, Qizhan ^a  

^a NANJING MEDICAL UNIVERSITY   (China)

^b GUIZHOU MEDICAL UNIVERSITY   (China)

Author keywords

Arsenite; Cancer stem cell like properties; Epigenetic regulation; Let 7c; Neoplastic transformation

Indexed keywords

ARSENIC TRIOXIDE; CARCINOGEN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LET 7A; LET 7B; LET 7C; RAS PROTEIN; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CANCER CELL CULTURE; CANCER CELL HACAT; CANCER STEM CELL; CARCINOGENICITY; CELL LINE; CELL STRUCTURE; DNA METHYLATION; ENVIRONMENTAL EXPOSURE; EPIGENETIC REPRESSION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; KERATINOCYTE; MALIGNANT TRANSFORMATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION;

ARSENITE; CANCER STEM CELL-LIKE PROPERTIES; EPIGENETIC REGULATION; LET-7C; NEOPLASTIC TRANSFORMATION;

ANIMALS; ARSENITES; AZACITIDINE; CELL LINE; CELL TRANSFORMATION, NEOPLASTIC; EPIGENESIS, GENETIC; GENE SILENCING; HUMANS; KERATINOCYTES; MICE; MICE, NUDE; MICRORNAS; NEOPLASTIC STEM CELLS; NF-KAPPA B; RAS PROTEINS; SODIUM COMPOUNDS;

EID: 84899071428     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2014.03.020     Document Type: Article

References (41)

1. Baer C., Claus R., Plass C. Genome-wide epigenetic regulation of miRNAs in cancer. Cancer Res. 2013, 73:473-477.
2. Basseres D.S., Ebbs A., Levantini E., Baldwin A.S. Requirement of the NF-kappaB subunit p65/RelA for K-Ras-induced lung tumorigenesis. Cancer Res. 2010, 70:3537-3546.
3. Benitah S.A. Tumour biology: skin-cancer stem cells outwitted. Nature 2011, 478:329-330.
4. Bolt H.M. Arsenic: an ancient toxicant of continuous public health impact, from Iceman Otzi until now. Arch. Toxicol. 2012, 86:825-830.
5. Brueckner B., Stresemann C., Kuner R., Mund C., Musch T., Meister M., Sultmann H., Lyko F. The human let-7a-3 locus contains an epigenetically regulated microRNA gene with oncogenic function. Cancer Res. 2007, 67:1419-1423.
6. Childs G., Fazzari M., Kung G., Kawachi N., Brandwein-Gensler M., McLemore M., Chen Q., Burk R.D., Smith R.V., Prystowsky M.B., Belbin T.J., Schlecht N.F. Low-level expression of microRNAs let-7d and miR-205 are prognostic markers of head and neck squamous cell carcinoma. Am. J. Pathol. 2009, 174:736-745.
7. Chou C.K., Liang K.H., Tzeng C.C., Huang G.C., Chuang J.I., Chang T.Y., Liu H.S. Dominant-negative Rac1 suppresses Ras-induced apoptosis possibly through activation of NFkappaB in Ha-ras oncogene-transformed NIH/3T3 cells. Life Sci. 2006, 78:1823-1829.
8. Cullen B.R. Assaying nuclear messenger RNA export in human cells. Methods Mol. Biol. 2004, 257:85-92.
9. Eaves C.J. Cancer stem cells: here, there, everywhere?. Nature 2008, 456:581-582.
10. Fusenig N.E., Boukamp P. Multiple stages and genetic alterations in immortalization, malignant transformation, and tumor progression of human skin keratinocytes. Mol. Carcinog. 1998, 23:144-158.
11. Hayashi Y., Tsujii M., Wang J., Kondo J., Akasaka T., Jin Y., Li W., Nakamura T., Nishida T., Iijima H., Tsuji S., Kawano S., Hayashi N., Takehara T. CagA mediates epigenetic regulation to attenuate let-7 expression in Helicobacter pylori-related carcinogenesis. Gut 2012, 0:1-11.
12. Hutvagner G., Zamore P.D. A microRNA in a multiple-turnover RNAi enzyme complex. Science 2002, 297:2056-2060.
13. Jensen T.J., Novak P., Eblin K.E., Gandolfi A.J., Futscher B.W. Epigenetic remodeling during arsenical-induced malignant transformation. Carcinogenesis 2008, 29:1500-1508.
14. Jiang R., Li Y., Xu Y., Zhou Y., Pang Y., Shen L., Zhao Y., Zhang J., Zhou J., Wang X., Liu Q. EMT and CSC-like properties mediated by the IKKbeta/IkappaBalpha/RelA signal pathway via the transcriptional regulator, Snail, are involved in the arsenite-induced neoplastic transformation of human keratinocytes. Arch. Toxicol. 2013, 87:991-1000.
15. Johnson S.M., Grosshans H., Shingara J., Byrom M., Jarvis R., Cheng A., Labourier E., Reinert K.L., Brown D., Slack F.J. RAS is regulated by the let-7 microRNA family. Cell 2005, 120:635-647.
16. Kasinski A.L., Slack F.J. Potential microRNA therapies targeting Ras, NFkappaB and p53 signaling. Curr. Opin. Mol. Ther. 2010, 12:147-157.
17. Kim B.Y., Gaynor R.B., Song K., Dritschilo A., Jung M. Constitutive activation of NF-kappaB in Ki-ras-transformed prostate epithelial cells. Oncogene 2002, 21:4490-4497.
18. Kim H.M., Haraguchi N., Ishii H., Ohkuma M., Okano M., Mimori K., Eguchi H., Yamamoto H., Nagano H., Sekimoto M., Doki Y., Mori M. Increased CD13 expression reduces reactive oxygen species, promoting survival of liver cancer stem cells via an epithelial-mesenchymal transition-like phenomenon. Ann. Surg. Oncol. 2011, 19(Suppl 3):S539-S548.
19. Komissarova E.V., Rossman T.G. Arsenite induced poly(ADP-ribosyl)ation of tumor suppressor P53 in human skin keratinocytes as a possible mechanism for carcinogenesis associated with arsenic exposure. Toxicol. Appl. Pharmacol. 2010, 243:399-404.
20. Li Y., Ling M., Xu Y., Wang S., Li Z., Zhou J., Wang X., Liu Q. The repressive effect of NF-kappaB on p53 by mot-2 is involved in human keratinocyte transformation induced by low levels of arsenite. Toxicol. Sci. 2010, 116:174-182.
21. Li Y., VandenBoom T.G., Kong D., Wang Z., Ali S., Philip P.A., Sarkar F.H. Up-regulation of miR-200 and let-7 by natural agents leads to the reversal of epithelial-to-mesenchymal transition in gemcitabine-resistant pancreatic cancer cells. Cancer Res. 2009, 69:6704-6712.
22. Lin T., Meng L., Li Y., Tsai R.Y. Tumor-initiating function of nucleostemin-enriched mammary tumor cells. Cancer Res. 2010, 70:9444-9452.
23. Liu C., Kelnar K., Vlassov A.V., Brown D., Wang J., Tang D.G. Distinct microRNA expression profiles in prostate cancer stem/progenitor cells and tumor-suppressive functions of let-7. Cancer Res. 2012, 72:3393-3404.
24. Liu Y., Lyle S., Yang Z., Cotsarelis G. Keratin 15 promoter targets putative epithelial stem cells in the hair follicle bulge. J. Invest. Dermatol. 2003, 121:963-968.
25. Lu L., Katsaros D., de la Longrais I.A., Sochirca O., Yu H. Hypermethylation of let-7a-3 in epithelial ovarian cancer is associated with low insulin-like growth factor-II expression and favorable prognosis. Cancer Res. 2007, 67:10117-10122.
26. McCarty M.F. Metformin may antagonize Lin28 and/or Lin28B activity, thereby boosting let-7 levels and antagonizing cancer progression. Med. Hypotheses 2012, 78:262-269.
27. Melton C., Judson R.L., Blelloch R. Opposing microRNA families regulate self-renewal in mouse embryonic stem cells. Nature 2010, 463:621-626.
28. Mitin N., Kudla A.J., Konieczny S.F., Taparowsky E.J. Differential effects of Ras signaling through NFkappaB on skeletal myogenesis. Oncogene 2001, 20:1276-1286.
29. Mitra D., Das P.M., Huynh F.C., Jones F.E. Jumonji/ARID1 B (JARID1B) protein promotes breast tumor cell cycle progression through epigenetic repression of microRNA let-7e. J. Biol. Chem. 2011, 286:40531-40535.
30. Nemoto Y., Maruo T., Sato T., Deguchi T., Ito T., Sugiyama H., Ishikawa T., Madarame H., Watanabe T., Shida T., Sahara H. Identification of cancer stem cells derived from a canine lung adenocarcinoma cell line. Vet. Pathol. 2011, 48:1029-1034.
31. Pi J., Diwan B.A., Sun Y., Liu J., Qu W., He Y., Styblo M., Waalkes M.P. Arsenic-induced malignant transformation of human keratinocytes: involvement of Nrf2. Free Radic. Biol. Med. 2008, 45:651-658.
32. Sakurai M., Miki Y., Masuda M., Hata S., Shibahara Y., Hirakawa H., Suzuki T., Sasano H. LIN28: a regulator of tumor-suppressing activity of let-7 microRNA in human breast cancer. J. Steroid Biochem. Mol. Biol. 2012, 131:101-106.
33. Su P.F., Hu Y.J., Ho I.C., Cheng Y.M., Lee T.C. Distinct gene expression profiles in immortalized human urothelial cells exposed to inorganic arsenite and its methylated trivalent metabolites. Environ. Health Perspect. 2006, 114:394-403.
34. Takebe N., Warren R.Q., Ivy S.P. Breast cancer growth and metastasis: interplay between cancer stem cells, embryonic signaling pathways and epithelial-to-mesenchymal transition. Breast Cancer Res. 2011, 13:211.
35. Tokar E.J., Diwan B.A., Waalkes M.P. Arsenic exposure transforms human epithelial stem/progenitor cells into a cancer stem-like phenotype. Environ Health. Perspect. 2010, 118:108-115.
36. Trempus C.S., Morris R.J., Ehinger M., Elmore A., Bortner C.D., Ito M., Cotsarelis G., Nijhof J.G., Peckham J., Flagler N., Kissling G., Humble M.M., King L.C., Adams L.D., Desai D., Amin S., Tennant R.W. CD34 expression by hair follicle stem cells is required for skin tumor development in mice. Cancer Res. 2007, 67:4173-4181.
37. Vasilatou D., Papageorgiou S., Dimitriadis G., Pappa V. Epigenetic alterations and microRNAs: new players in the pathogenesis of myelodysplastic syndromes. Epigenetics 2013, 8:561-570.
38. Wang Z., Zhao Y., Smith E., Goodall G.J., Drew P.A., Brabletz T., Yang C. Reversal and prevention of arsenic-induced human bronchial epithelial cell malignant transformation by microRNA-200b. Toxicol. Sci. 2011, 121:110-122.
39. Xia X.M., Jin W.Y., Shi R.Z., Zhang Y.F., Chen J. Clinical significance and the correlation of expression between Let-7 and K-ras in non-small cell lung cancer. Oncol. Lett. 2010, 1:1045-1047.
40. Xu Y., Li Y., Pang Y., Ling M., Shen L., Jiang R., Zhao Y., Zhou J., Wang X., Liu Q. Blockade of p53 by HIF-2alpha, but not HIF-1alpha, is involved in arsenite-induced malignant transformation of human bronchial epithelial cells. Arch. Toxicol. 2012, 86:947-959.
41. Zhang D., Ma Q., Wang Z., Zhang M., Guo K., Wang F., Wu E. beta2-adrenoceptor blockage induces G1/S phase arrest and apoptosis in pancreatic cancer cells via Ras/Akt/NFkappaB pathway. Mol. Cancer 2011, 10:146.