Epithelial-mesenchymal transition and cancer stem cells, mediated by a long non-coding RNA, HOTAIR, are involved in cell malignant transformation induced by cigarette smoke extract

Toxicology and Applied Pharmacology

Volumn 282, Issue 1, 2015, Pages 9-19

  Liu, Yi ^a   Luo, Fei ^a   Xu, Yuan ^a   Wang, Bairu ^a   Zhao, Yue ^a   Xu, Wenchao ^a   Shi, Le ^a   Lu, Xiaolin ^a   Liu, Qizhan ^a  

^a NANJING MEDICAL UNIVERSITY   (China)

Author keywords

Cancer stem cells (CSCs); Carcinogenesis; Cigarette smoke extract (CSE); Epithelial mesenchymal transition (EMT); Inflammation; LncRNAs

Indexed keywords

CIGARETTE SMOKE; CIGARETTE SMOKE CONDENSATE; HOX PROTEIN; INTERLEUKIN 6; LONG UNTRANSLATED RNA; STAT3 PROTEIN; HOTAIR LONG UNTRANSLATED RNA, HUMAN; IL6 PROTEIN, HUMAN; SMOKE; STAT3 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER STEM CELL; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; HUMAN; HUMAN CELL; LUNG CARCINOGENESIS; MALIGNANT TRANSFORMATION; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN INTERACTION; SIGNAL TRANSDUCTION; UPREGULATION; ADVERSE EFFECTS; ANIMAL; AUTOCRINE EFFECT; CELL TRANSFORMATION; DOSE RESPONSE; DRUG EFFECTS; EPITHELIUM CELL; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; LUNG; LUNG NEOPLASMS; METABOLISM; NUDE MOUSE; PATHOLOGY; RNA INTERFERENCE; SMOKE; SMOKING; TIME; TRANSFORMED CELL LINE;

ANIMALS; AUTOCRINE COMMUNICATION; CELL LINE, TRANSFORMED; CELL TRANSFORMATION, NEOPLASTIC; DOSE-RESPONSE RELATIONSHIP, DRUG; EPITHELIAL CELLS; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INTERLEUKIN-6; LUNG; LUNG NEOPLASMS; MICE; MICE, NUDE; NEOPLASTIC STEM CELLS; RNA INTERFERENCE; RNA, LONG NONCODING; SIGNAL TRANSDUCTION; SMOKE; SMOKING; STAT3 TRANSCRIPTION FACTOR; TIME FACTORS; TRANSFECTION; UP-REGULATION;

EID: 84911377275     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2014.10.022     Document Type: Article

References (63)

1. Balkwill F.R., Mantovani A. Cancer-related inflammation: common themes and therapeutic opportunities. Semin. Cancer Biol. 2012, 22:33-40.
2. Baum B., Settleman J., Quinlan M.P. Transitions between epithelial and mesenchymal states in development and disease. Semin. Cell Dev. Biol. 2008, 19:294-308.
3. Besaratinia A., Pfeifer G.P. Second-hand smoke and human lung cancer. Lancet Oncol. 2008, 9:657-666.
4. Brabletz T., Jung A., Spaderna S., Hlubek F., Kirchner T. Opinion: migrating cancer stem cells - an integrated concept of malignant tumour progression. Nat. Rev. Cancer 2005, 5:744-749.
5. Chen B., Liu J., Chang Q., Beezhold K., Lu Y., Chen F. JNK and STAT3 signaling pathways converge on Akt-mediated phosphorylation of EZH2 in bronchial epithelial cells induced by arsenic. Cell Cycle 2013, 12:112-121.
6. Chen J., Wang J., Lin L., He L., Wu Y., Zhang L., Yi Z., Chen Y., Pang X., Liu M. Inhibition of STAT3 signaling pathway by nitidine chloride suppressed the angiogenesis and growth of human gastric cancer. Mol. Cancer Ther. 2012, 11:277-287.
7. Chen L.F., Williams S.A., Mu Y., Nakano H., Duerr J.M., Buckbinder L., Greene W.C. NF-kappaB RelA phosphorylation regulates RelA acetylation. Mol. Cell. Biol. 2005, 25:7966-7975.
8. Chen W., Xu X., Bai L., Padilla M.T., Gott K.M., Leng S., Tellez C.S., Wilder J.A., Belinsky S.A., Scott B.R., Lin Y. Low-dose gamma-irradiation inhibits IL-6 secretion from human lung fibroblasts that promotes bronchial epithelial cell transformation by cigarette-smoke carcinogen. Carcinogenesis 2012, 33:1368-1374.
9. Derrien T., Johnson R., Bussotti G., Tanzer A., Djebali S., Tilgner H., Guernec G., Martin D., Merkel A., Knowles D.G., Lagarde J., Veeravalli L., Ruan X., Ruan Y., Lassmann T., Carninci P., Brown J.B., Lipovich L., Gonzalez J.M., Thomas M., Davis C.A., Shiekhattar R., Gingeras T.R., Hubbard T.J., Notredame C., Harrow J., Guigo R. The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res. 2012, 22:1775-1789.
10. Dohadwala M., Wang G., Heinrich E., Luo J., Lau O., Shih H., Munaim Q., Lee G., Hong L., Lai C., Abemayor E., Fishbein M.C., Elashoff D.A., Dubinett S.M., St John M.A. The role of ZEB1 in the inflammation-induced promotion of EMT in HNSCC. Otolaryngology--head and neck surgery. J. Am. Acad. Otolaryngol. Head Neck Surg. 2010, 142:753-759.
11. Eramo A., Lotti F., Sette G., Pilozzi E., Biffoni M., Di Virgilio A., Conticello C., Ruco L., Peschle C., De Maria R. Identification and expansion of the tumorigenic lung cancer stem cell population. Cell Death Differ. 2008, 15:504-514.
12. Geng Y.J., Xie S.L., Li Q., Ma J., Wang G.Y. Large intervening non-coding RNA HOTAIR is associated with hepatocellular carcinoma progression. J. Int. Med. Res. 2011, 39:2119-2128.
13. Gibb E.A., Vucic E.A., Enfield K.S., Stewart G.L., Lonergan K.M., Kennett J.Y., Becker-Santos D.D., MacAulay C.E., Lam S., Brown C.J., Lam W.L. Human cancer long non-coding RNA transcriptomes. PLoS One 2011, 6:e25915.
14. Gupta R.A., Shah N., Wang K.C., Kim J., Horlings H.M., Wong D.J., Tsai M.C., Hung T., Argani P., Rinn J.L., Wang Y., Brzoska P., Kong B., Li R., West R.B., van de Vijver M.J., Sukumar S., Chang H.Y. Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature 2010, 464:1071-1076.
15. Guttman M., Donaghey J., Carey B.W., Garber M., Grenier J.K., Munson G., Young G., Lucas A.B., Ach R., Bruhn L., Yang X., Amit I., Meissner A., Regev A., Rinn J.L., Root D.E., Lander E.S. lincRNAs act in the circuitry controlling pluripotency and differentiation. Nature 2011, 477:295-300.
16. Ho P.L., Lay E.J., Jian W., Parra D., Chan K.S. Stat3 activation in urothelial stem cells leads to direct progression to invasive bladder cancer. Cancer Res. 2012, 72:3135-3142.
17. Hochedlinger K., Yamada Y., Beard C., Jaenisch R. Ectopic expression of Oct-4 blocks progenitor-cell differentiation and causes dysplasia in epithelial tissues. Cell 2005, 121:465-477.
18. Ji P., Diederichs S., Wang W., Boing S., Metzger R., Schneider P.M., Tidow N., Brandt B., Buerger H., Bulk E., Thomas M., Berdel W.E., Serve H., Muller-Tidow C. MALAT-1, a novel noncoding RNA, and thymosin beta4 predict metastasis and survival in early-stage non-small cell lung cancer. Oncogene 2003, 22:8031-8041.
19. Kobrinsky N.L., Klug M.G., Hokanson P.J., Sjolander D.E., Burd L. Impact of smoking on cancer stage at diagnosis. J. Clin. Oncol. Off. J. Am. Soc. Clin. Oncol. 2003, 21:907-913.
20. Kogo R., Shimamura T., Mimori K., Kawahara K., Imoto S., Sudo T., Tanaka F., Shibata K., Suzuki A., Komune S., Miyano S., Mori M. Long noncoding RNA HOTAIR regulates polycomb-dependent chromatin modification and is associated with poor prognosis in colorectal cancers. Cancer Res. 2011, 71:6320-6326.
21. Lee T.I., Johnstone S.E., Young R.A. Chromatin immunoprecipitation and microarray-based analysis of protein location. Nat. Protoc. 2006, 1:729-748.
22. Lesmes G.R., Donofrio K.H. Passive smoking: the medical and economic issues. Am. J. Med. 1992, 93:38S-42S.
23. Leung E.L., Fiscus R.R., Tung J.W., Tin V.P., Cheng L.C., Sihoe A.D., Fink L.M., Ma Y., Wong M.P. Non-small cell lung cancer cells expressing CD44 are enriched for stem cell-like properties. PLoS One 2010, 5:e14062.
24. Li X., Wu Z., Fu X., Han W. Long noncoding RNAs: insights from biological features and functions to diseases. Med. Res. Rev. 2013, 33:517-553.
25. Liu W., Xie S., Chen X., Rao X., Ren H., Hu B., Yin T., Xiang Y., Ren J. Activation of the IL-6/JAK/STAT3 signaling pathway in human middle ear cholesteatoma epithelium. Int. J. Clin. Exp. Pathol. 2014, 7:709-715.
26. Luo F., Xu Y., Ling M., Zhao Y., Xu W., Liang X., Jiang R., Wang B., Bian Q., Liu Q. Arsenite evokes IL-6 secretion, autocrine regulation of STAT3 signaling, and miR-21 expression, processes involved in the EMT and malignant transformation of human bronchial epithelial cells. Toxicol. Appl. Pharmacol. 2013, 273:27-34.
27. Mani S.A., Guo W., Liao M.J., Eaton E.N., Ayyanan A., Zhou A.Y., Brooks M., Reinhard F., Zhang C.C., Shipitsin M., Campbell L.L., Polyak K., Brisken C., Yang J., Weinberg R.A. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008, 133:704-715.
28. Martin L., Chang H.Y. Uncovering the role of genomic "dark matter" in human disease. J. Clin. Invest. 2012, 122:1589-1595.
29. Mayer G., Raddatz M.S., Grunwald J.D., Famulok M. RNA ligands that distinguish metabolite-induced conformations in the TPP riboswitch. Angew. Chem. Int. Ed. Engl. 2007, 46:557-560.
30. Montelius M., Ljungberg M., Horn M., Forssell-Aronsson E. Tumour size measurement in a mouse model using high resolution MRI. BMC Med. Imaging 2012, 12:12.
31. Mourtada-Maarabouni M., Pickard M.R., Hedge V.L., Farzaneh F., Williams G.T. GAS5, a non-protein-coding RNA, controls apoptosis and is downregulated in breast cancer. Oncogene 2009, 28:195-208.
32. Niinuma T., Suzuki H., Nojima M., Nosho K., Yamamoto H., Takamaru H., Yamamoto E., Maruyama R., Nobuoka T., Miyazaki Y., Nishida T., Bamba T., Kanda T., Ajioka Y., Taguchi T., Okahara S., Takahashi H., Nishida Y., Hosokawa M., Hasegawa T., Tokino T., Hirata K., Imai K., Toyota M., Shinomura Y. Upregulation of miR-196a and HOTAIR drive malignant character in gastrointestinal stromal tumors. Cancer Res. 2012, 72:1126-1136.
33. Ozgur E., Mert U., Isin M., Okutan M., Dalay N., Gezer U. Differential expression of long non-coding RNAs during genotoxic stress-induced apoptosis in HeLa and MCF-7 cells. Clin. Exp. med. 2013, 13:119-126.
34. Padua Alves C., Fonseca A.S., Muys B.R., de Barros E.L.B.R., Burger M.C., de Souza J.E., Valente V., Zago M.A., Silva W.A. Brief report: The lincRNA Hotair is required for epithelial-to-mesenchymal transition and stemness maintenance of cancer cell lines. Stem Cells 2013, 31:2827-2832.
35. Parsons A., Daley A., Begh R., Aveyard P. Influence of smoking cessation after diagnosis of early stage lung cancer on prognosis: systematic review of observational studies with meta-analysis. BMJ 2010, 340:b5569.
36. Pauli A., Rinn J.L., Schier A.F. Non-coding RNAs as regulators of embryogenesis. Nat. Rev. Genet. 2011, 12:136-149.
37. Pawlus M.R., Wang L., Hu C.J. STAT3 and HIF1alpha cooperatively activate HIF1 target genes in MDA-MB-231 and RCC4 cells. Oncogene 2014, 33:1670-1679.
38. Peinado H., Portillo F., Cano A. Transcriptional regulation of cadherins during development and carcinogenesis. Int. J. Dev. Biol. 2004, 48:365-375.
39. Puxbaum V., Nimmerfall E., Bauerl C., Taub N., Blaas P.M., Wieser J., Mikula M., Mikulits W., Ng K.M., Yeoh G.C., Mach L. M6P/IGF2R modulates the invasiveness of liver cells via its capacity to bind mannose 6-phosphate residues. J. Hepatol. 2012, 57:337-343.
40. Rathinavelu A., Narasimhan M., Muthumani P. A novel regulation of VEGF expression by HIF-1alpha and STAT3 in HDM2 transfected prostate cancer cells. J. Cell. Mol. Med. 2012, 16:1750-1757.
41. Reddel R.R., Ke Y., Gerwin B.I., McMenamin M.G., Lechner J.F., Su R.T., Brash D.E., Park J.B., Rhim J.S., Harris C.C. Transformation of human bronchial epithelial cells by infection with SV40 or adenovirus-12 SV40 hybrid virus, or transfection via strontium phosphate coprecipitation with a plasmid containing SV40 early region genes. Cancer Res. 1988, 48:1904-1909.
42. Rinn J.L., Kertesz M., Wang J.K., Squazzo S.L., Xu X., Brugmann S.A., Goodnough L.H., Helms J.A., Farnham P.J., Segal E., Chang H.Y. Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 2007, 129:1311-1323.
43. Rokavec M., Oner M.G., Li H., Jackstadt R., Jiang L., Lodygin D., Kaller M., Horst D., Ziegler P.K., Schwitalla S., Slotta-Huspenina J., Bader F.G., Greten F.R., Hermeking H. IL-6R/STAT3/miR-34a feedback loop promotes EMT-mediated colorectal cancer invasion and metastasis. J. Clin. Invest. 2014, 124:1853-1867.
44. Sasco A.J., Secretan M.B., Straif K. Tobacco smoking and cancer: a brief review of recent epidemiological evidence. Lung Cancer 2004, 45(Suppl. 2):S3-S9.
45. Saxena A., Carninci P. Long non-coding RNA modifies chromatin: epigenetic silencing by long non-coding RNAs. Bioessays 2011, 33:830-839.
46. Shuang Z.Y., Wu W.C., Xu J., Lin G., Liu Y.C., Lao X.M., Zheng L., Li S. Transforming growth factor-beta1-induced epithelial-mesenchymal transition generates ALDH-positive cells with stem cell properties in cholangiocarcinoma. Cancer Lett. 2014, 354:320-328.
47. Thai P., Statt S., Chen C.H., Liang E., Campbell C., Wu R. Characterization of a novel long noncoding RNA, SCAL1, induced by cigarette smoke and elevated in lung cancer cell lines. Am. J. Respir. Cell Mol. Biol. 2013, 49:204-211.
48. van Bakel H., Hughes T.R. Establishing legitimacy and function in the new transcriptome. Funct. Genom. Proteome 2009, 8:424-436.
49. Wang B., Yang H., Huang Y.Z., Yan R.H., Liu F.J., Zhang J.N. Biologic characteristics of the side population of human small cell lung cancer cell line H446. Chin. J. Cancer 2010, 29:254-260.
50. Wang Y., Xu Z., Jiang J., Xu C., Kang J., Xiao L., Wu M., Xiong J., Guo X., Liu H. Endogenous miRNA sponge lincRNA-RoR regulates Oct4, Nanog, and Sox2 in human embryonic stem cell self-renewal. Dev. Cell 2013, 25:69-80.
51. Wapinski O., Chang H.Y. Long noncoding RNAs and human disease. Trends Cell Biol. 2011, 21:354-361.
52. Woo C.J., Kingston R.E. HOTAIR lifts noncoding RNAs to new levels. Cell 2007, 129:1257-1259.
53. Wu Z.H., Wang X.L., Tang H.M., Jiang T., Chen J., Lu S., Qiu G.Q., Peng Z.H., Yan D.W. Long non-coding RNA HOTAIR is a powerful predictor of metastasis and poor prognosis and is associated with epithelial-mesenchymal transition in colon cancer. Oncol. Rep. 2014, 32:395-402.
54. Xu Y., Li Y., Li H., Pang Y., Zhao Y., Jiang R., Shen L., Zhou J., Wang X., Liu Q. The accumulations of HIF-1alpha and HIF-2alpha by JNK and ERK are involved in biphasic effects induced by different levels of arsenite in human bronchial epithelial cells. Toxicol. Appl. Pharmacol. 2013, 266:187-197.
55. Xu Y., Li Y., Pang Y., Ling M., Shen L., Yang X., Zhang J., Zhou J., Wang X., Liu Q. EMT and stem cell-like properties associated with HIF-2alpha are involved in arsenite-induced transformation of human bronchial epithelial cells. PLoS One 2012, 7:e37765.
56. Yang J., Weinberg R.A. Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev. Cell 2008, 14:818-829.
57. Yang M.H., Hsu D.S., Wang H.W., Wang H.J., Lan H.Y., Yang W.H., Huang C.H., Kao S.Y., Tzeng C.H., Tai S.K., Chang S.Y., Lee O.K., Wu K.J. Bmi1 is essential in Twist1-induced epithelial-mesenchymal transition. Nat. Cell Biol. 2010, 12:982-992.
58. Yang Z., Zhou L., Wu L.M., Lai M.C., Xie H.Y., Zhang F., Zheng S.S. Overexpression of long non-coding RNA HOTAIR predicts tumor recurrence in hepatocellular carcinoma patients following liver transplantation. Ann. Surg. Oncol. 2011, 18:1243-1250.
59. Yoon J.H., Abdelmohsen K., Srikantan S., Yang X., Martindale J.L., De S., Huarte M., Zhan M., Becker K.G., Gorospe M. LincRNA-p21 suppresses target mRNA translation. Mol. Cell 2012, 47:648-655.
60. Zhang L.J., Liu W., Gao Y.M., Qin Y.J., Wu R.D. The expression of IL-6 and STAT3 might predict progression and unfavorable prognosis in Wilms' tumor. Biochem. Biophys. Res. Commun. 2013, 435:408-413.
61. Zhao Y., Xu Y., Li Y., Xu W., Luo F., Wang B., Pang Y., Xiang Q., Zhou J., Wang X., Liu Q. NF-kappaB-mediated inflammation leading to EMT via miR-200c is involved in cell transformation induced by cigarette smoke extract. Toxicol. Sci. J. Soc. Toxicol. 2013, 135:265-276.
62. Zhou C., Liu J., Tang Y., Liang X. Inflammation linking EMT and cancer stem cells. Oral Oncol. 2012, 48:1068-1075.
63. Zhu D., Wan X., Huang H., Chen X., Liang W., Zhao F., Lin T., Han J., Xie W. Knockdown of Bmi1 inhibits the stemness properties and tumorigenicity of human bladder cancer stem cell-like side population cells. Oncol. Rep. 2014, 31:727-736.