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Published in: Tumor Biology 2/2016

01-02-2016 | Original Article

Long non-coding RNA MALAT1 modulates radiosensitivity of HR-HPV+ cervical cancer via sponging miR-145

Authors: Hongzhi Lu, Yu He, Lin Lin, Zhengqin Qi, Li Ma, Li Li, Ying Su

Published in: Tumor Biology | Issue 2/2016

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Abstract

Metastasis-associated lung adenocarcinoma transcript 1 (MALAT1) is a lncRNA playing oncogenic role in several cancers, including cervical cancer. However, its role in radiosensitivity of cervical cancer is not yet well understood. This study explored the role of MALAT1 in radiosensitivity of high-risk human papillomavirus (HR-HPV)-positive cervical cancer and whether there is a ceRNA mechanism which participated in its regulation over radiosensitivity. Based on tissue samples from 50 cervical cancer cases and 25 healthy controls, we found MALAT1 expression was significantly higher in radioresistant than in radiosensitive cancer cases. In addition, MALAT1 and miR-145 expression inversely changed in response to irradiation in HR-HPV+ cervical cancer cells. By using clonogenic assay and flow cytometry analysis of cell cycle distribution and apoptosis, we found CaSki and Hela cells with knockdown of MALAT1 had significantly lower colony formation, higher ratio of G2/M phase block and higher ratio of cell apoptosis. By performing RNA-binding protein immunoprecipitation (RIP) assay and RNA pull-down assay, we confirmed that miR-145 and MALAT1 were in the same Ago2 complex and there was a reciprocal repression between them. Then, we explored the function of MALAT1-miR-145 in radiosensitivity of cervical cancers cells and demonstrated that si-MALAT1 and miR-145 had some level of synergic effect in reducing cancer cell colony formation, cell cycle regulation, and inducing apoptosis. These findings provide an important clue about microRNA-lncRNA interaction in the mechanism of radioresistance of cervical cancer.
Literature
1.
go back to reference Siegel R, Ma J, Zou Z, Jemal A. Cancer statistics, 2014. CA: a Cancer Journal for Clinicians. 2014;64:9–29. Siegel R, Ma J, Zou Z, Jemal A. Cancer statistics, 2014. CA: a Cancer Journal for Clinicians. 2014;64:9–29.
2.
go back to reference Rogers L, Siu SS, Luesley D, Bryant A, Dickinson HO. Radiotherapy and chemoradiation after surgery for early cervical cancer. The Cochrane Database of Systematic Reviews. 2012;5, CD007583.PubMedCentral Rogers L, Siu SS, Luesley D, Bryant A, Dickinson HO. Radiotherapy and chemoradiation after surgery for early cervical cancer. The Cochrane Database of Systematic Reviews. 2012;5, CD007583.PubMedCentral
3.
go back to reference Powell ME. Modern radiotherapy and cervical cancer. International Journal of Gynecological Cancer : Official Journal of the International Gynecological Cancer Society. 2010;20:S49–51.CrossRef Powell ME. Modern radiotherapy and cervical cancer. International Journal of Gynecological Cancer : Official Journal of the International Gynecological Cancer Society. 2010;20:S49–51.CrossRef
4.
go back to reference Munagala R, Kausar H, Munjal C, Gupta RC. Withaferin A induces p53-dependent apoptosis by repression of HPV oncogenes and upregulation of tumor suppressor proteins in human cervical cancer cells. Carcinogenesis. 2011;32:1697–705.CrossRefPubMed Munagala R, Kausar H, Munjal C, Gupta RC. Withaferin A induces p53-dependent apoptosis by repression of HPV oncogenes and upregulation of tumor suppressor proteins in human cervical cancer cells. Carcinogenesis. 2011;32:1697–705.CrossRefPubMed
5.
go back to reference Lando M, Holden M, Bergersen LC, Svendsrud DH, Stokke T, Sundfor K, et al. Gene dosage, expression, and ontology analysis identifies driver genes in the carcinogenesis and chemoradioresistance of cervical cancer. PLoS Genetics. 2009;5, e1000719.CrossRefPubMedPubMedCentral Lando M, Holden M, Bergersen LC, Svendsrud DH, Stokke T, Sundfor K, et al. Gene dosage, expression, and ontology analysis identifies driver genes in the carcinogenesis and chemoradioresistance of cervical cancer. PLoS Genetics. 2009;5, e1000719.CrossRefPubMedPubMedCentral
8.
go back to reference Gibb EA, Becker-Santos DD, Enfield KS, Guillaud M, Niekerk D, Matisic JP, et al. Aberrant expression of long noncoding RNAs in cervical intraepithelial neoplasia. International Journal of Gynecological Cancer: Official Journal of the International Gynecological Cancer Society. 2012;22:1557–63.CrossRef Gibb EA, Becker-Santos DD, Enfield KS, Guillaud M, Niekerk D, Matisic JP, et al. Aberrant expression of long noncoding RNAs in cervical intraepithelial neoplasia. International Journal of Gynecological Cancer: Official Journal of the International Gynecological Cancer Society. 2012;22:1557–63.CrossRef
9.
go back to reference Yin DD, Liu ZJ, Zhang E, Kong R, Zhang ZH, Guo RH. Decreased expression of long noncoding RNA MEG3 affects cell proliferation and predicts a poor prognosis in patients with colorectal cancer. Tumour Biology: the Journal of the International Society for Oncodevelopmental Biology and Medicine. 2015;36:4851–9.CrossRef Yin DD, Liu ZJ, Zhang E, Kong R, Zhang ZH, Guo RH. Decreased expression of long noncoding RNA MEG3 affects cell proliferation and predicts a poor prognosis in patients with colorectal cancer. Tumour Biology: the Journal of the International Society for Oncodevelopmental Biology and Medicine. 2015;36:4851–9.CrossRef
10.
go back to reference Sun M, Xia R, Jin F, Xu T, Liu Z, De W, et al. Downregulated long noncoding RNA MEG3 is associated with poor prognosis and promotes cell proliferation in gastric cancer. Tumour Biology: the Journal of the International Society for Oncodevelopmental Biology and Medicine. 2014;35:1065–73.CrossRef Sun M, Xia R, Jin F, Xu T, Liu Z, De W, et al. Downregulated long noncoding RNA MEG3 is associated with poor prognosis and promotes cell proliferation in gastric cancer. Tumour Biology: the Journal of the International Society for Oncodevelopmental Biology and Medicine. 2014;35:1065–73.CrossRef
11.
go back to reference Ying L, Huang Y, Chen H, Wang Y, Xia L, Chen Y, et al. Downregulated MEG3 activates autophagy and increases cell proliferation in bladder cancer. Molecular BioSystems. 2013;9:407–11.CrossRefPubMed Ying L, Huang Y, Chen H, Wang Y, Xia L, Chen Y, et al. Downregulated MEG3 activates autophagy and increases cell proliferation in bladder cancer. Molecular BioSystems. 2013;9:407–11.CrossRefPubMed
12.
go back to reference Qin R, Chen Z, Ding Y, Hao J, Hu J, Guo F. Long non-coding RNA MEG3 inhibits the proliferation of cervical carcinoma cells through the induction of cell cycle arrest and apoptosis. Neoplasma. 2013;60:486–92.CrossRefPubMed Qin R, Chen Z, Ding Y, Hao J, Hu J, Guo F. Long non-coding RNA MEG3 inhibits the proliferation of cervical carcinoma cells through the induction of cell cycle arrest and apoptosis. Neoplasma. 2013;60:486–92.CrossRefPubMed
13.
go back to reference Jiang Y, Li Y, Fang S, Jiang B, Qin C, Xie P, et al. The role of MALAT1 correlates with HPV in cervical cancer. Oncology Letters. 2014;7:2135–41.PubMedPubMedCentral Jiang Y, Li Y, Fang S, Jiang B, Qin C, Xie P, et al. The role of MALAT1 correlates with HPV in cervical cancer. Oncology Letters. 2014;7:2135–41.PubMedPubMedCentral
14.
go back to reference Liu S, Song L, Zeng S, Zhang L. MALAT1-miR-124-RBG2 axis is involved in growth and invasion of HR-HPV-positive cervical cancer cells. Tumour Biology: the Journal of the International Society for Oncodevelopmental Biology and Medicine. 2015. Liu S, Song L, Zeng S, Zhang L. MALAT1-miR-124-RBG2 axis is involved in growth and invasion of HR-HPV-positive cervical cancer cells. Tumour Biology: the Journal of the International Society for Oncodevelopmental Biology and Medicine. 2015.
15.
go back to reference Zhang J, Wang L, Li B, Huo M, Mu M, Liu J, et al. miR-145 downregulates the expression of cyclin-dependent kinase 6 in human cervical carcinoma cells. Experimental and Therapeutic Medicine. 2014;8:591–4.PubMedPubMedCentral Zhang J, Wang L, Li B, Huo M, Mu M, Liu J, et al. miR-145 downregulates the expression of cyclin-dependent kinase 6 in human cervical carcinoma cells. Experimental and Therapeutic Medicine. 2014;8:591–4.PubMedPubMedCentral
16.
go back to reference Chang S, Gao L, Yang Y, Tong D, Guo B, Liu L, et al. miR-145 mediates the antiproliferative and gene regulatory effects of vitamin D3 by directly targeting E2F3 in gastric cancer cells. Oncotarget. 2015;6:7675–85.CrossRefPubMedPubMedCentral Chang S, Gao L, Yang Y, Tong D, Guo B, Liu L, et al. miR-145 mediates the antiproliferative and gene regulatory effects of vitamin D3 by directly targeting E2F3 in gastric cancer cells. Oncotarget. 2015;6:7675–85.CrossRefPubMedPubMedCentral
17.
go back to reference Qiu T, Zhou X, Wang J, Du Y, Xu J, Huang Z, et al. MiR-145, miR-133a and miR-133b inhibit proliferation, migration, invasion and cell cycle progression via targeting transcription factor Sp1 in gastric cancer. FEBS Letters. 2014;588:1168–77.CrossRefPubMed Qiu T, Zhou X, Wang J, Du Y, Xu J, Huang Z, et al. MiR-145, miR-133a and miR-133b inhibit proliferation, migration, invasion and cell cycle progression via targeting transcription factor Sp1 in gastric cancer. FEBS Letters. 2014;588:1168–77.CrossRefPubMed
18.
go back to reference Koh WJ, Greer BE, Abu-Rustum NR, Apte SM, Campos SM, Chan J, et al. National Comprehensive Cancer Network: cervical cancer. Journal of the National Comprehensive Cancer Network: JNCCN. 2013;11:320–43.CrossRefPubMed Koh WJ, Greer BE, Abu-Rustum NR, Apte SM, Campos SM, Chan J, et al. National Comprehensive Cancer Network: cervical cancer. Journal of the National Comprehensive Cancer Network: JNCCN. 2013;11:320–43.CrossRefPubMed
19.
go back to reference Liu Q, Huang J, Zhou N, Zhang Z, Zhang A, Lu Z, et al. LncRNA loc285194 is a p53-regulated tumor suppressor. Nucleic Acids Research. 2013;41:4976–87.CrossRefPubMedPubMedCentral Liu Q, Huang J, Zhou N, Zhang Z, Zhang A, Lu Z, et al. LncRNA loc285194 is a p53-regulated tumor suppressor. Nucleic Acids Research. 2013;41:4976–87.CrossRefPubMedPubMedCentral
20.
go back to reference Zhang A, Zhou N, Huang J, Liu Q, Fukuda K, Ma D, et al. The human long non-coding RNA-RoR is a p53 repressor in response to DNA damage. Cell Research. 2013;23:340–50.CrossRefPubMed Zhang A, Zhou N, Huang J, Liu Q, Fukuda K, Ma D, et al. The human long non-coding RNA-RoR is a p53 repressor in response to DNA damage. Cell Research. 2013;23:340–50.CrossRefPubMed
21.
go back to reference Gregory RI, Chendrimada TP, Cooch N, Shiekhattar R. Human RISC couples microRNA biogenesis and posttranscriptional gene silencing. Cell. 2005;123:631–40.CrossRefPubMed Gregory RI, Chendrimada TP, Cooch N, Shiekhattar R. Human RISC couples microRNA biogenesis and posttranscriptional gene silencing. Cell. 2005;123:631–40.CrossRefPubMed
22.
go back to reference Karginov FV, Conaco C, Xuan Z, Schmidt BH, Parker JS, Mandel G, et al. A biochemical approach to identifying microRNA targets. Proceedings of the National Academy of Sciences of the United States of America. 2007;104:19291–6.CrossRefPubMedPubMedCentral Karginov FV, Conaco C, Xuan Z, Schmidt BH, Parker JS, Mandel G, et al. A biochemical approach to identifying microRNA targets. Proceedings of the National Academy of Sciences of the United States of America. 2007;104:19291–6.CrossRefPubMedPubMedCentral
23.
go back to reference Gutschner T, Hammerle M, Eissmann M, Hsu J, Kim Y, Hung G, et al. The noncoding RNA MALAT1 is a critical regulator of the metastasis phenotype of lung cancer cells. Cancer Research. 2013;73:1180–9.CrossRefPubMed Gutschner T, Hammerle M, Eissmann M, Hsu J, Kim Y, Hung G, et al. The noncoding RNA MALAT1 is a critical regulator of the metastasis phenotype of lung cancer cells. Cancer Research. 2013;73:1180–9.CrossRefPubMed
24.
go back to reference Ji Q, Zhang L, Liu X, Zhou L, Wang W, Han Z, et al. Long non-coding RNA MALAT1 promotes tumour growth and metastasis in colorectal cancer through binding to SFPQ and releasing oncogene PTBP2 from SFPQ/PTBP2 complex. British Journal of Cancer. 2014;111:736–48.CrossRefPubMedPubMedCentral Ji Q, Zhang L, Liu X, Zhou L, Wang W, Han Z, et al. Long non-coding RNA MALAT1 promotes tumour growth and metastasis in colorectal cancer through binding to SFPQ and releasing oncogene PTBP2 from SFPQ/PTBP2 complex. British Journal of Cancer. 2014;111:736–48.CrossRefPubMedPubMedCentral
25.
go back to reference Wang J, Su L, Chen X, Li P, Cai Q, Yu B, et al. MALAT1 promotes cell proliferation in gastric cancer by recruiting SF2/ASF. Biomedicine & Pharmacotherapy = Biomedecine & Pharmacotherapie. 2014;68:557–64.CrossRef Wang J, Su L, Chen X, Li P, Cai Q, Yu B, et al. MALAT1 promotes cell proliferation in gastric cancer by recruiting SF2/ASF. Biomedicine & Pharmacotherapy = Biomedecine & Pharmacotherapie. 2014;68:557–64.CrossRef
26.
go back to reference Yang F, Yi F, Han X, Du Q, Liang Z. MALAT-1 interacts with hnRNP C in cell cycle regulation. FEBS Letters. 2013;587:3175–81.CrossRefPubMed Yang F, Yi F, Han X, Du Q, Liang Z. MALAT-1 interacts with hnRNP C in cell cycle regulation. FEBS Letters. 2013;587:3175–81.CrossRefPubMed
27.
go back to reference Wang X, Li M, Wang Z, Han S, Tang X, Ge Y, et al. Silencing of long noncoding RNA MALAT1 by miR-101 and miR-217 inhibits proliferation, migration, and invasion of esophageal squamous cell carcinoma cells. The Journal of Biological Chemistry. 2015;290:3925–35.CrossRefPubMed Wang X, Li M, Wang Z, Han S, Tang X, Ge Y, et al. Silencing of long noncoding RNA MALAT1 by miR-101 and miR-217 inhibits proliferation, migration, and invasion of esophageal squamous cell carcinoma cells. The Journal of Biological Chemistry. 2015;290:3925–35.CrossRefPubMed
28.
go back to reference Bandopadhyay M, Banerjee A, Sarkar N, Panigrahi R, Datta S, Pal A, et al. Tumor suppressor micro RNA miR-145 and onco micro RNAs miR-21 and miR-222 expressions are differentially modulated by hepatitis B virus X protein in malignant hepatocytes. BMC Cancer. 2014;14:721.CrossRefPubMedPubMedCentral Bandopadhyay M, Banerjee A, Sarkar N, Panigrahi R, Datta S, Pal A, et al. Tumor suppressor micro RNA miR-145 and onco micro RNAs miR-21 and miR-222 expressions are differentially modulated by hepatitis B virus X protein in malignant hepatocytes. BMC Cancer. 2014;14:721.CrossRefPubMedPubMedCentral
29.
go back to reference Eades G, Wolfson B, Zhang Y, Li Q, Yao Y, Zhou Q. LincRNA-RoR and miR-145 regulate invasion in triple-negative breast cancer via targeting ARF6. Molecular cancer research: MCR. 2015;13:330–8.CrossRefPubMed Eades G, Wolfson B, Zhang Y, Li Q, Yao Y, Zhou Q. LincRNA-RoR and miR-145 regulate invasion in triple-negative breast cancer via targeting ARF6. Molecular cancer research: MCR. 2015;13:330–8.CrossRefPubMed
30.
go back to reference Shen H, Shen J, Wang L, Shi Z, Wang M, Jiang BH, et al. Low miR-145 expression level is associated with poor pathological differentiation and poor prognosis in non-small cell lung cancer. Biomedicine & Pharmacotherapy = Biomedecine & Pharmacotherapie. 2015;69:301–5.CrossRef Shen H, Shen J, Wang L, Shi Z, Wang M, Jiang BH, et al. Low miR-145 expression level is associated with poor pathological differentiation and poor prognosis in non-small cell lung cancer. Biomedicine & Pharmacotherapy = Biomedecine & Pharmacotherapie. 2015;69:301–5.CrossRef
31.
go back to reference Chang, S., Gao, L., Yang, Y., Tong, D., Guo, B., Liu, L., Li, Z., Song, T., and Huang C. 2015. miR-145 mediates the antiproliferative and gene regulatory effects of vitamin D3 by directly targeting E2F3 in gastric cancer cells. Oncotarget. Chang, S., Gao, L., Yang, Y., Tong, D., Guo, B., Liu, L., Li, Z., Song, T., and Huang C. 2015. miR-145 mediates the antiproliferative and gene regulatory effects of vitamin D3 by directly targeting E2F3 in gastric cancer cells. Oncotarget.
32.
go back to reference Xue G, Ren Z, Chen Y, Zhu J, Du Y, Pan D, et al. A feedback regulation between miR-145 and DNA methyltransferase 3b in prostate cancer cell and their responses to irradiation. Cancer Letters. 2015;361:121–7.CrossRefPubMed Xue G, Ren Z, Chen Y, Zhu J, Du Y, Pan D, et al. A feedback regulation between miR-145 and DNA methyltransferase 3b in prostate cancer cell and their responses to irradiation. Cancer Letters. 2015;361:121–7.CrossRefPubMed
33.
go back to reference Shi M, Du L, Liu D, Qian L, Hu M, Yu M, et al. Glucocorticoid regulation of a novel HPV-E6-p53-miR-145 pathway modulates invasion and therapy resistance of cervical cancer cells. The Journal of Pathology. 2012;228:148–57.CrossRefPubMed Shi M, Du L, Liu D, Qian L, Hu M, Yu M, et al. Glucocorticoid regulation of a novel HPV-E6-p53-miR-145 pathway modulates invasion and therapy resistance of cervical cancer cells. The Journal of Pathology. 2012;228:148–57.CrossRefPubMed
34.
go back to reference Hansen TB, Jensen TI, Clausen BH, Bramsen JB, Finsen B, Damgaard CK, et al. Natural RNA circles function as efficient microRNA sponges. Nature. 2013;495:384–8.CrossRefPubMed Hansen TB, Jensen TI, Clausen BH, Bramsen JB, Finsen B, Damgaard CK, et al. Natural RNA circles function as efficient microRNA sponges. Nature. 2013;495:384–8.CrossRefPubMed
Metadata
Title
Long non-coding RNA MALAT1 modulates radiosensitivity of HR-HPV+ cervical cancer via sponging miR-145
Authors
Hongzhi Lu
Yu He
Lin Lin
Zhengqin Qi
Li Ma
Li Li
Ying Su
Publication date
01-02-2016
Publisher
Springer Netherlands
Published in
Tumor Biology / Issue 2/2016
Print ISSN: 1010-4283
Electronic ISSN: 1423-0380
DOI
https://doi.org/10.1007/s13277-015-3946-5

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