Skip to main content
Erschienen in: Cellular Oncology 6/2016

28.09.2016 | Original Paper

Identification of genetic variation in the lncRNA HOTAIR associated with HPV16-related cervical cancer pathogenesis

verfasst von: Sweta Sharma Saha, Rahul Roy Chowdhury, Nidhu Ranjan Mondal, Biman Chakravarty, Tanmay Chatterjee, Sudipta Roy, Sharmila Sengupta

Erschienen in: Cellular Oncology | Ausgabe 6/2016

Einloggen, um Zugang zu erhalten

Abstract

Purpose

Previously, over-expression of the long noncoding RNA (lncRNA) HOTAIR has been found to be associated with the invasive and metastatic capacities of several epithelial cancers, including cervical cancer (CaCx). Here, we aimed at identifying functionally relevant genetic variants that may be employed to differentiate between clinically distinct CaCx subtypes, i.e., those exhibiting high HOTAIR levels and molecular signatures of metastasis and those lacking such signatures in the presence of low HOTAIR expression levels.

Methods

Genomic DNA isolated from various cervical tissue samples (characterized by histopathology and HPV status) was used for HOTAIR amplicon sequencing, followed by validation of the findings by Sanger sequencing. The impact of the genetic variants found on the secondary structure of HOTAIR and the concomitant alterations in miRNA binding sites were determined through in silico analysis, followed by miRNA expression analysis by quantitative real-time PCR and confirmation of miRNA binding using a luciferase reporter assay.

Results

We found that rs2366152C was over-represented [ORage-adjusted = 2.58 (1.23–5.57); p = 0.014] in low HOTAIR expressing HPV positive CaCx cases compared to HPV negative controls. This genetic variant showed the propensity of a secondary structure alteration and gain of a miR-22 binding site in HOTAIR, which was found to be concordant with miR-22 over-expression in low HOTAIR CaCx cases compared to controls. We found that miR-22 expression negatively correlated with HOTAIR and E7 expression in HPV16 positive cases and in an E7 transfected HPV negative CaCx-derived cell line (C33A), but was not altered in high HOTAIR cases compared to controls. Reduced luciferase activity of a HOTAIR rs2366152C expression plasmid in C33A cells through miR-22 co-transfection confirmed the ability of miR-22 to specifically target rs2366152C-harbouring HOTAIR lncRNA in CaCx cells, ultimately leading to its down-regulation.

Conclusions

Our data indicate that rs2366152C not only has the potential to serve as a marker for singling out CaCx cases lacking metastatic molecular signatures, but also to explain the functional inactivation of HOTAIR in these cases, including the mechanism of its down-regulation.
Anhänge
Nur mit Berechtigung zugänglich
Literatur
1.
Zurück zum Zitat J. Ferlay, I. Soerjomataram, M. Ervik, R. Dikshit, S. Eser, C. Mathers, M. Rebelo, D.M. Parkin, D. Forman, F. Bray, GLOBOCAN 2012 v1.0, cancer incidence and mortality worldwide: IARC cancer base no. 11 [internet] (International Agency for Research on Cancer, Lyon, 2013). Available from: http://globocan.iarc.fr. Accessed Dec 2015 J. Ferlay, I. Soerjomataram, M. Ervik, R. Dikshit, S. Eser, C. Mathers, M. Rebelo, D.M. Parkin, D. Forman, F. Bray, GLOBOCAN 2012 v1.0, cancer incidence and mortality worldwide: IARC cancer base no. 11 [internet] (International Agency for Research on Cancer, Lyon, 2013). Available from: http://​globocan.​iarc.​fr. Accessed Dec 2015
2.
Zurück zum Zitat Guidelines for cervical cancer screening programme. Government of India - World Health Organization Collaboration Programme 2004–2005 (2006) Guidelines for cervical cancer screening programme. Government of India - World Health Organization Collaboration Programme 2004–2005 (2006)
3.
Zurück zum Zitat H. zur Hausen, Papillomavirus infections–a major cause of human cancers. Biochim. Biophys. Acta 1288, F55–F78 (1996)PubMed H. zur Hausen, Papillomavirus infections–a major cause of human cancers. Biochim. Biophys. Acta 1288, F55–F78 (1996)PubMed
4.
Zurück zum Zitat P. Pisani, D.M. Parkin, F. Bray, J. Ferlay, Estimates of the worldwide mortality from 25 cancers in 1990. Int. J. Cancer 83, 18–29 (1999)CrossRefPubMed P. Pisani, D.M. Parkin, F. Bray, J. Ferlay, Estimates of the worldwide mortality from 25 cancers in 1990. Int. J. Cancer 83, 18–29 (1999)CrossRefPubMed
5.
Zurück zum Zitat F.X. Bosch, M.M. Manos, N. Muñoz, M. Sherman, A.M. Jansen, J. Peto, M.H. Schiffman, V. Moreno, R. Kurman, K.V. Shah, Prevalence of human papillomavirus DNA in cervical cancer: a worldwide perspective. International biological study on cervical cancer (IBSCC) study group. J. Natl. Cancer Inst. 87, 796–802 (1995)CrossRefPubMed F.X. Bosch, M.M. Manos, N. Muñoz, M. Sherman, A.M. Jansen, J. Peto, M.H. Schiffman, V. Moreno, R. Kurman, K.V. Shah, Prevalence of human papillomavirus DNA in cervical cancer: a worldwide perspective. International biological study on cervical cancer (IBSCC) study group. J. Natl. Cancer Inst. 87, 796–802 (1995)CrossRefPubMed
6.
Zurück zum Zitat J.M. Walboomers, M.V. Jacobs, M.M. Manos, F.X. Bosch, J.A. Kummer, K.V. Shah, P.J. Snijders, J. Peto, C.J. Meijer, N. Muñoz, Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J. Pathol. 189, 12–19 (1999)CrossRefPubMed J.M. Walboomers, M.V. Jacobs, M.M. Manos, F.X. Bosch, J.A. Kummer, K.V. Shah, P.J. Snijders, J. Peto, C.J. Meijer, N. Muñoz, Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J. Pathol. 189, 12–19 (1999)CrossRefPubMed
7.
Zurück zum Zitat S.B. Prasad, S.S. Yadav, M. Das, A. Modi, S. Kumari, L.K. Pandey, S. Singh, S. Pradhan, G. Narayan, PI3K/AKT pathway-mediated regulation of p27(Kip1) is associated with cell cycle arrest and apoptosis in cervical cancer. Cell. Oncol. 38, 215–225 (2015)CrossRef S.B. Prasad, S.S. Yadav, M. Das, A. Modi, S. Kumari, L.K. Pandey, S. Singh, S. Pradhan, G. Narayan, PI3K/AKT pathway-mediated regulation of p27(Kip1) is associated with cell cycle arrest and apoptosis in cervical cancer. Cell. Oncol. 38, 215–225 (2015)CrossRef
8.
Zurück zum Zitat H. Romanczuk, P.M. Howley, Disruption of either the E1 or the E2 regulatory gene of human papillomavirus type 16 increases viral immortalization capacity. Proc. Natl. Acad. Sci. U. S. A. 89, 3159–3163 (1992)CrossRefPubMedPubMedCentral H. Romanczuk, P.M. Howley, Disruption of either the E1 or the E2 regulatory gene of human papillomavirus type 16 increases viral immortalization capacity. Proc. Natl. Acad. Sci. U. S. A. 89, 3159–3163 (1992)CrossRefPubMedPubMedCentral
9.
Zurück zum Zitat M. Narisawa-Saito, T. Kiyono, Basic mechanisms of high-risk human papillomavirus-induced carcinogenesis: roles of E6 and E7 proteins. Cancer Sci. 98, 1505–1511 (2007)CrossRefPubMed M. Narisawa-Saito, T. Kiyono, Basic mechanisms of high-risk human papillomavirus-induced carcinogenesis: roles of E6 and E7 proteins. Cancer Sci. 98, 1505–1511 (2007)CrossRefPubMed
10.
Zurück zum Zitat S. Chellappan, V.B. Kraus, B. Kroger, K. Munger, P.M. Howley, W.C. Phelps, J.R. Nevins, Adenovirus ElA, simian virus 40 tumor antigen, and human papillomavirus E7 protein share the capacity to disrupt the interaction between transcription factor E2F and the retinoblastoma gene product. Proc. Natl. Acad. Sci. U. S. A. 89, 4549–4553 (1992)CrossRefPubMedPubMedCentral S. Chellappan, V.B. Kraus, B. Kroger, K. Munger, P.M. Howley, W.C. Phelps, J.R. Nevins, Adenovirus ElA, simian virus 40 tumor antigen, and human papillomavirus E7 protein share the capacity to disrupt the interaction between transcription factor E2F and the retinoblastoma gene product. Proc. Natl. Acad. Sci. U. S. A. 89, 4549–4553 (1992)CrossRefPubMedPubMedCentral
11.
Zurück zum Zitat S. Sharma, P. Mandal, T. Sadhukhan, R. Roy Chowdhury, N. Ranjan Mondal, B. Chakravarty, T. Chatterjee, S. Roy, S. Sengupta, Bridging links between long noncoding RNA HOTAIR and HPV oncoprotein E7 in cervical cancer pathogenesis. Sci. Rep. 5, 11724 (2015)CrossRefPubMedPubMedCentral S. Sharma, P. Mandal, T. Sadhukhan, R. Roy Chowdhury, N. Ranjan Mondal, B. Chakravarty, T. Chatterjee, S. Roy, S. Sengupta, Bridging links between long noncoding RNA HOTAIR and HPV oncoprotein E7 in cervical cancer pathogenesis. Sci. Rep. 5, 11724 (2015)CrossRefPubMedPubMedCentral
12.
Zurück zum Zitat C.P. Ponting, P.L. Oliver, W. Reik, Evolution and functions of long noncoding RNAs. Cell 136, 629–641 (2009)CrossRefPubMed C.P. Ponting, P.L. Oliver, W. Reik, Evolution and functions of long noncoding RNAs. Cell 136, 629–641 (2009)CrossRefPubMed
14.
Zurück zum Zitat M. Vitiello, A. Tuccoli, L. Poliseno, Long non-coding RNAs in cancer: implications for personalized therapy. Cell. Oncol. 38, 17–28 (2015)CrossRef M. Vitiello, A. Tuccoli, L. Poliseno, Long non-coding RNAs in cancer: implications for personalized therapy. Cell. Oncol. 38, 17–28 (2015)CrossRef
15.
Zurück zum Zitat J.L. Rinn, M. Kertesz, J.K. Wang, S.L. Squazzo, X. Xu, S.A. Brugmann, L.H. Goodnough, J.A. Helms, P.J. Farnham, E. Segal, H.Y. Chang, Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 129, 1311–1323 (2007)CrossRefPubMedPubMedCentral J.L. Rinn, M. Kertesz, J.K. Wang, S.L. Squazzo, X. Xu, S.A. Brugmann, L.H. Goodnough, J.A. Helms, P.J. Farnham, E. Segal, H.Y. Chang, Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 129, 1311–1323 (2007)CrossRefPubMedPubMedCentral
16.
Zurück zum Zitat U.A. Ørom, T. Derrien, M. Beringer, K. Gumireddy, A. Gardini, G. Bussotti, F. Lai, M. Zytnicki, C. Notredame, Q. Huang, R. Guigo, R. Shiekhattar, Long noncoding RNAs with enhancer-like function in human cells. Cell 143, 46–58 (2010)CrossRefPubMedPubMedCentral U.A. Ørom, T. Derrien, M. Beringer, K. Gumireddy, A. Gardini, G. Bussotti, F. Lai, M. Zytnicki, C. Notredame, Q. Huang, R. Guigo, R. Shiekhattar, Long noncoding RNAs with enhancer-like function in human cells. Cell 143, 46–58 (2010)CrossRefPubMedPubMedCentral
17.
Zurück zum Zitat M.E. Dinger, P.P. Amaral, T.R. Mercer, K.C. Pang, S.J. Bruce, B.B. Gardiner, M.E. Askarian-Amiri, K. Ru, G. Soldà, C. Simons, S.M. Sunkin, M.L. Crowe, S.M. Grimmond, A.C. Perkins, J.S. Mattick, Long noncoding RNAs in mouse embryonic stem cell pluripotency and differentiation. Genome Res. 18, 1433–1445 (2008)CrossRefPubMedPubMedCentral M.E. Dinger, P.P. Amaral, T.R. Mercer, K.C. Pang, S.J. Bruce, B.B. Gardiner, M.E. Askarian-Amiri, K. Ru, G. Soldà, C. Simons, S.M. Sunkin, M.L. Crowe, S.M. Grimmond, A.C. Perkins, J.S. Mattick, Long noncoding RNAs in mouse embryonic stem cell pluripotency and differentiation. Genome Res. 18, 1433–1445 (2008)CrossRefPubMedPubMedCentral
18.
Zurück zum Zitat T. Nagano, P. Fraser, No-nonsense functions for long noncoding RNAs. Cell 145, 178–181 (2011)CrossRefPubMed T. Nagano, P. Fraser, No-nonsense functions for long noncoding RNAs. Cell 145, 178–181 (2011)CrossRefPubMed
19.
Zurück zum Zitat V. Taucher, H. Mangge, J. Haybaeck, Non-coding RNAs in pancreatic cancer: challenges and opportunities for clinical application. Cell. Oncol. 39, 295–318 (2016)CrossRef V. Taucher, H. Mangge, J. Haybaeck, Non-coding RNAs in pancreatic cancer: challenges and opportunities for clinical application. Cell. Oncol. 39, 295–318 (2016)CrossRef
21.
Zurück zum Zitat R.A. Gupta, N. Shah, K.C. Wang, J. Kim, H.M. Horlings, D.J. Wong, M.C. Tsai, T. Hung, P. Argani, J.L. Rinn, Y. Wang, P. Brzoska, B. Kong, R. Li, R.B. West, M.J. van de Vijver, S. Sukumar, H.Y. Chang, Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature 464, 1071–1076 (2010)CrossRefPubMedPubMedCentral R.A. Gupta, N. Shah, K.C. Wang, J. Kim, H.M. Horlings, D.J. Wong, M.C. Tsai, T. Hung, P. Argani, J.L. Rinn, Y. Wang, P. Brzoska, B. Kong, R. Li, R.B. West, M.J. van de Vijver, S. Sukumar, H.Y. Chang, Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature 464, 1071–1076 (2010)CrossRefPubMedPubMedCentral
22.
Zurück zum Zitat M.-C. Tsai, O. Manor, Y. Wan, N. Mosammaparast, J.K. Wang, F. Lan, Y. Shi, E. Segal, H.Y. Chang, Long noncoding RNA as modular scaffold of histone modification complexes. Science 329, 689–693 (2010)CrossRefPubMedPubMedCentral M.-C. Tsai, O. Manor, Y. Wan, N. Mosammaparast, J.K. Wang, F. Lan, Y. Shi, E. Segal, H.Y. Chang, Long noncoding RNA as modular scaffold of histone modification complexes. Science 329, 689–693 (2010)CrossRefPubMedPubMedCentral
23.
Zurück zum Zitat A. Ferraro, Altered primary chromatin structures and their implications in cancer development. Cell. Oncol. 39, 195–210 (2016)CrossRef A. Ferraro, Altered primary chromatin structures and their implications in cancer development. Cell. Oncol. 39, 195–210 (2016)CrossRef
24.
Zurück zum Zitat R. Kogo, T. Shimamura, K. Mimori, K. Kawahara, S. Imoto, T. Sudo, F. Tanaka, K. Shibata, A. Suzuki, S. Komune, S. Miyano, M. Mori, Long noncoding RNA HOTAIR regulates polycomb-dependent chromatin modification and is associated with poor prognosis in colorectal cancers. Cancer Res. 71, 6320–6326 (2011)CrossRefPubMed R. Kogo, T. Shimamura, K. Mimori, K. Kawahara, S. Imoto, T. Sudo, F. Tanaka, K. Shibata, A. Suzuki, S. Komune, S. Miyano, M. Mori, Long noncoding RNA HOTAIR regulates polycomb-dependent chromatin modification and is associated with poor prognosis in colorectal cancers. Cancer Res. 71, 6320–6326 (2011)CrossRefPubMed
25.
Zurück zum Zitat X. Li, Z. Wu, Q. Mei, X. Li, M. Guo, X. Fu, W. Han, Long non-coding RNA HOTAIR, a driver of malignancy, predicts negative prognosis and exhibits oncogenic activity in oesophageal squamous cell carcinoma. Br. J. Cancer 109, 2266–2278 (2013)CrossRefPubMedPubMedCentral X. Li, Z. Wu, Q. Mei, X. Li, M. Guo, X. Fu, W. Han, Long non-coding RNA HOTAIR, a driver of malignancy, predicts negative prognosis and exhibits oncogenic activity in oesophageal squamous cell carcinoma. Br. J. Cancer 109, 2266–2278 (2013)CrossRefPubMedPubMedCentral
26.
Zurück zum Zitat M. Ishibashi, R. Kogo, K. Shibata, G. Sawada, Y. Takahashi, J. Kurashige, S. Akiyoshi, S. Sasaki, T. Iwaya, T. Sudo, K. Sugimachi, K. Mimori, G. Wakabayashi, M. Mori, Clinical significance of the expression of long non-coding RNA HOTAIR in primary hepatocellular carcinoma. Oncol. Rep. 29, 946–950 (2013)PubMed M. Ishibashi, R. Kogo, K. Shibata, G. Sawada, Y. Takahashi, J. Kurashige, S. Akiyoshi, S. Sasaki, T. Iwaya, T. Sudo, K. Sugimachi, K. Mimori, G. Wakabayashi, M. Mori, Clinical significance of the expression of long non-coding RNA HOTAIR in primary hepatocellular carcinoma. Oncol. Rep. 29, 946–950 (2013)PubMed
27.
Zurück zum Zitat Z.H. Wu, X.L. Wang, H.M. Tang, T. Jiang, J. Chen, S. Lu, G.Q. Qiu, Z.H. Peng, D.W. Yan, 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. 32, 395–402 (2014)PubMed Z.H. Wu, X.L. Wang, H.M. Tang, T. Jiang, J. Chen, S. Lu, G.Q. Qiu, Z.H. Peng, D.W. Yan, 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. 32, 395–402 (2014)PubMed
28.
Zurück zum Zitat L. Huang, L.M. Liao, A.W. Liu, J.B. Wu, X.L. Cheng, J.X. Lin, M. Zheng, Overexpression of long noncoding RNA HOTAIR predicts a poor prognosis in patients with cervical cancer. Arch. Gynecol. Obstet. 290, 717–723 (2014)CrossRefPubMed L. Huang, L.M. Liao, A.W. Liu, J.B. Wu, X.L. Cheng, J.X. Lin, M. Zheng, Overexpression of long noncoding RNA HOTAIR predicts a poor prognosis in patients with cervical cancer. Arch. Gynecol. Obstet. 290, 717–723 (2014)CrossRefPubMed
29.
Zurück zum Zitat H.J. Kim, D.W. Lee, G.W. Yim, E.J. Nam, S. Kim, S.W. Kim, Y.T. Kim, Long non-coding RNA HOTAIR is associated with human cervical cancer progression. Int. J. Oncol. 46, 521–530 (2014)PubMedPubMedCentral H.J. Kim, D.W. Lee, G.W. Yim, E.J. Nam, S. Kim, S.W. Kim, Y.T. Kim, Long non-coding RNA HOTAIR is associated with human cervical cancer progression. Int. J. Oncol. 46, 521–530 (2014)PubMedPubMedCentral
30.
Zurück zum Zitat X. Zhang, L. Zhou, G. Fu, F. Sun, J. Shi, J. Wei, C. Lu, C. Zhou, Q. Yuan, M. Yang, The identification of an ESCC susceptibility SNP rs920778 that regulates the expression of lncRNA HOTAIR via a novel intronic enhancer. Carcinogenesis 35, 2062–2067 (2014)CrossRefPubMed X. Zhang, L. Zhou, G. Fu, F. Sun, J. Shi, J. Wei, C. Lu, C. Zhou, Q. Yuan, M. Yang, The identification of an ESCC susceptibility SNP rs920778 that regulates the expression of lncRNA HOTAIR via a novel intronic enhancer. Carcinogenesis 35, 2062–2067 (2014)CrossRefPubMed
31.
Zurück zum Zitat W. Pan, L. Liu, J. Wei, Y. Ge, J. Zhang, H. Chen, L. Zhou, Q. Yuan, C. Zhou, M. Yang, A functional lncRNA HOTAIR genetic variant contributes to gastric cancer susceptibility. Mol. Carcinog 55, 90–96 (2015)CrossRefPubMed W. Pan, L. Liu, J. Wei, Y. Ge, J. Zhang, H. Chen, L. Zhou, Q. Yuan, C. Zhou, M. Yang, A functional lncRNA HOTAIR genetic variant contributes to gastric cancer susceptibility. Mol. Carcinog 55, 90–96 (2015)CrossRefPubMed
32.
Zurück zum Zitat Y. Xue, D. Gu, G. Ma, L. Zhu, Q. Hua, H. Chu, N. Tong, J. Chen, Z. Zhang, M. Wang, Genetic variants in lncRNA HOTAIR are associated with risk of colorectal cancer. Mutagenesis 30, 303–310 (2015)CrossRefPubMed Y. Xue, D. Gu, G. Ma, L. Zhu, Q. Hua, H. Chu, N. Tong, J. Chen, Z. Zhang, M. Wang, Genetic variants in lncRNA HOTAIR are associated with risk of colorectal cancer. Mutagenesis 30, 303–310 (2015)CrossRefPubMed
33.
Zurück zum Zitat M. Du, W. Wang, H. Jin, Q. Wang, Y. Ge, J. Lu, G. Ma, H. Chu, N. Tong, H. Zhu, M. Wang, F. Qiang, Z. Zhang, The association analysis of lncRNA HOTAIR genetic variants and gastric cancer risk in a Chinese population. Oncotarget 6, 31255–31262 (2015)PubMedPubMedCentral M. Du, W. Wang, H. Jin, Q. Wang, Y. Ge, J. Lu, G. Ma, H. Chu, N. Tong, H. Zhu, M. Wang, F. Qiang, Z. Zhang, The association analysis of lncRNA HOTAIR genetic variants and gastric cancer risk in a Chinese population. Oncotarget 6, 31255–31262 (2015)PubMedPubMedCentral
34.
Zurück zum Zitat B. Bhattacharjee, S. Sengupta, HPV16 E2 gene disruption and polymorphisms of E2 and LCR: some significant associations with cervical cancer in Indian women. Gynecol. Oncol. 100, 372–378 (2006)CrossRefPubMed B. Bhattacharjee, S. Sengupta, HPV16 E2 gene disruption and polymorphisms of E2 and LCR: some significant associations with cervical cancer in Indian women. Gynecol. Oncol. 100, 372–378 (2006)CrossRefPubMed
35.
Zurück zum Zitat P. Bhattacharya, S. Sengupta, Predisposition to HPV16/18-related cervical cancer because of proline homozygosity at codon 72 of p53 among Indian women is influenced by HLA-B*07 and homozygosity of HLA-DQB1*03. Tissue Antigens 70, 283–293 (2007)CrossRefPubMed P. Bhattacharya, S. Sengupta, Predisposition to HPV16/18-related cervical cancer because of proline homozygosity at codon 72 of p53 among Indian women is influenced by HLA-B*07 and homozygosity of HLA-DQB1*03. Tissue Antigens 70, 283–293 (2007)CrossRefPubMed
36.
Zurück zum Zitat P. Laikangbam, S. Sengupta, P. Bhattacharya, C. Duttagupta, T. Dhabali Singh, Y. Verma, S. Roy, R. Das, S. Mukhopadhyay, A comparative profile of the prevalence and age distribution of human papillomavirus type 16/18 infections among three states of India with focus on northeast India. Int. J. Gynecol. Cancer 17, 107–117 (2007)CrossRefPubMed P. Laikangbam, S. Sengupta, P. Bhattacharya, C. Duttagupta, T. Dhabali Singh, Y. Verma, S. Roy, R. Das, S. Mukhopadhyay, A comparative profile of the prevalence and age distribution of human papillomavirus type 16/18 infections among three states of India with focus on northeast India. Int. J. Gynecol. Cancer 17, 107–117 (2007)CrossRefPubMed
37.
Zurück zum Zitat P. Mandal, B. Bhattacharjee, D. Das Ghosh, N.R. Mondal, R. Roy Chowdhury, S. Roy, S. Sengupta, Differential expression of HPV16 L2 gene in cervical cancers harboring episomal HPV16 genomes: influence of synonymous and non-coding region variations. PLoS One 8, e65647 (2013)CrossRefPubMedPubMedCentral P. Mandal, B. Bhattacharjee, D. Das Ghosh, N.R. Mondal, R. Roy Chowdhury, S. Roy, S. Sengupta, Differential expression of HPV16 L2 gene in cervical cancers harboring episomal HPV16 genomes: influence of synonymous and non-coding region variations. PLoS One 8, e65647 (2013)CrossRefPubMedPubMedCentral
38.
Zurück zum Zitat J. Ghose, M. Sinha, E. Das, N.R. Jana, N.P. Bhattacharyya, Regulation of miR-146a by RelA/NFkB and p53 in STHdh(Q111)/Hdh(Q111) cells, a cell model of Huntington’s disease. PLoS One 6, e23837 (2011)CrossRefPubMedPubMedCentral J. Ghose, M. Sinha, E. Das, N.R. Jana, N.P. Bhattacharyya, Regulation of miR-146a by RelA/NFkB and p53 in STHdh(Q111)/Hdh(Q111) cells, a cell model of Huntington’s disease. PLoS One 6, e23837 (2011)CrossRefPubMedPubMedCentral
39.
Zurück zum Zitat S. Bhattacharjya, S. Nath, J. Ghose, G.P. Maiti, N. Biswas, S. Bandyopadhyay, C.K. Panda, N.P. Bhattacharyya, S. Roychoudhury, miR-125b promotes cell death by targeting spindle assembly checkpoint gene MAD1 and modulating mitotic progression. Cell Death Differ. 20, 430–442 (2013)CrossRefPubMed S. Bhattacharjya, S. Nath, J. Ghose, G.P. Maiti, N. Biswas, S. Bandyopadhyay, C.K. Panda, N.P. Bhattacharyya, S. Roychoudhury, miR-125b promotes cell death by targeting spindle assembly checkpoint gene MAD1 and modulating mitotic progression. Cell Death Differ. 20, 430–442 (2013)CrossRefPubMed
40.
Zurück zum Zitat S. Bucha, D. Mukhopadhyay, N.P. Bhattacharyya, Regulation of mitochondrial morphology and cell cycle by microRNA-214 targeting Mitofusin2. Biochem. Biophys. Res. Commun. 465, 797–802 (2015)CrossRefPubMed S. Bucha, D. Mukhopadhyay, N.P. Bhattacharyya, Regulation of mitochondrial morphology and cell cycle by microRNA-214 targeting Mitofusin2. Biochem. Biophys. Res. Commun. 465, 797–802 (2015)CrossRefPubMed
41.
Zurück zum Zitat C. Braconi, T. Kogure, N. Valeri, N. Huang, G. Nuovo, S. Costinean, M. Negrini, E. Miotto, C.M. Croce, T. Patel, microRNA-29 can regulate expression of the long non-coding RNA gene MEG3 in hepatocellular cancer. Oncogene 30, 4750–4756 (2011)CrossRefPubMedPubMedCentral C. Braconi, T. Kogure, N. Valeri, N. Huang, G. Nuovo, S. Costinean, M. Negrini, E. Miotto, C.M. Croce, T. Patel, microRNA-29 can regulate expression of the long non-coding RNA gene MEG3 in hepatocellular cancer. Oncogene 30, 4750–4756 (2011)CrossRefPubMedPubMedCentral
42.
Zurück zum Zitat T. Chiyomaru, S. Fukuhara, S. Saini, S. Majid, G. Deng, V. Shahryari, I. Chang, Y. Tanaka, H. Enokida, M. Nakagawa, R. Dahiya, S. Yamamura, Long non-coding RNA HOTAIR is targeted and regulated by miR-141 in human cancer cells. J. Biol. Chem. 289, 12550–12565 (2014)CrossRefPubMedPubMedCentral T. Chiyomaru, S. Fukuhara, S. Saini, S. Majid, G. Deng, V. Shahryari, I. Chang, Y. Tanaka, H. Enokida, M. Nakagawa, R. Dahiya, S. Yamamura, Long non-coding RNA HOTAIR is targeted and regulated by miR-141 in human cancer cells. J. Biol. Chem. 289, 12550–12565 (2014)CrossRefPubMedPubMedCentral
43.
Zurück zum Zitat Z. Zhao, R. Li, S. Sha, Q. Wang, W. Mao, T. Liu, Targeting HER3 with miR-450b-3p suppresses breast cancer cells proliferation. Cancer Biol. Ther. 15, 1404–1412 (2014)CrossRefPubMedPubMedCentral Z. Zhao, R. Li, S. Sha, Q. Wang, W. Mao, T. Liu, Targeting HER3 with miR-450b-3p suppresses breast cancer cells proliferation. Cancer Biol. Ther. 15, 1404–1412 (2014)CrossRefPubMedPubMedCentral
44.
Zurück zum Zitat T. Punga, R. Le Panse, M. Andersson, F. Truffault, S. Berrih-Aknin, A.R. Punga, Circulating miRNAs in myasthenia gravis: miR-150-5p as a new potential biomarker. Ann. Clin. Transl. Neurol. 1, 49–58 (2014)CrossRefPubMed T. Punga, R. Le Panse, M. Andersson, F. Truffault, S. Berrih-Aknin, A.R. Punga, Circulating miRNAs in myasthenia gravis: miR-150-5p as a new potential biomarker. Ann. Clin. Transl. Neurol. 1, 49–58 (2014)CrossRefPubMed
45.
Zurück zum Zitat T. Li, J. Xie, C. Shen, D. Cheng, Y. Shi, Z. Wu, Q. Zhan, X. Deng, H. Chen, B. Shen, C. Peng, H. Li, Z. Zhu, miR-150-5p inhibits hepatoma cell migration and invasion by targeting MMP14. PLoS One 9, e115577 (2014)CrossRefPubMedPubMedCentral T. Li, J. Xie, C. Shen, D. Cheng, Y. Shi, Z. Wu, Q. Zhan, X. Deng, H. Chen, B. Shen, C. Peng, H. Li, Z. Zhu, miR-150-5p inhibits hepatoma cell migration and invasion by targeting MMP14. PLoS One 9, e115577 (2014)CrossRefPubMedPubMedCentral
46.
Zurück zum Zitat L. Liu, Y. Jiang, H. Zhang, A.R. Greenlee, R. Yu, Q. Yang, miR-22 functions as a micro-oncogene in transformed human bronchial epithelial cells induced by anti-benzo[a]pyrene-7,8-diol-9,10-epoxide. Toxicol. In Vitro 24, 1168–1175 (2010)CrossRefPubMed L. Liu, Y. Jiang, H. Zhang, A.R. Greenlee, R. Yu, Q. Yang, miR-22 functions as a micro-oncogene in transformed human bronchial epithelial cells induced by anti-benzo[a]pyrene-7,8-diol-9,10-epoxide. Toxicol. In Vitro 24, 1168–1175 (2010)CrossRefPubMed
47.
Zurück zum Zitat S.J. Song, K. Ito, U. Ala, L. Kats, K. Webster, S.M. Sun, M. Jongen-Lavrencic, K. Manova-Todorova, J. Teruya-Feldstein, D.E. Avigan, R. Delwel, P.P. Pandolfi, The oncogenic microRNA miR-22 targets the TET2 tumor suppressor to promote hematopoietic stem cell self-renewal and transformation. Cell Stem Cell 13, 87–101 (2013)CrossRefPubMedPubMedCentral S.J. Song, K. Ito, U. Ala, L. Kats, K. Webster, S.M. Sun, M. Jongen-Lavrencic, K. Manova-Todorova, J. Teruya-Feldstein, D.E. Avigan, R. Delwel, P.P. Pandolfi, The oncogenic microRNA miR-22 targets the TET2 tumor suppressor to promote hematopoietic stem cell self-renewal and transformation. Cell Stem Cell 13, 87–101 (2013)CrossRefPubMedPubMedCentral
48.
Zurück zum Zitat L.-M. Kong, C.-G. Liao, Y. Zhang, J. Xu, Y. Li, W. Huang, Y. Zhang, H. Bian, Z.N. Chen, A regulatory loop involving miR-22, Sp1 and c-Myc modulates CD147 expression in breast cancer invasion and metastasis. Cancer Res. 74, 3764–3778 (2014)CrossRefPubMed L.-M. Kong, C.-G. Liao, Y. Zhang, J. Xu, Y. Li, W. Huang, Y. Zhang, H. Bian, Z.N. Chen, A regulatory loop involving miR-22, Sp1 and c-Myc modulates CD147 expression in breast cancer invasion and metastasis. Cancer Res. 74, 3764–3778 (2014)CrossRefPubMed
49.
Zurück zum Zitat W.N. Wan, Y.Q. Zhang, X.M. Wang, Y.J. Liu, Y.X. Zhang, Y.H. Que, W.J. Zhao, P. Li, Down-regulated miR-22 as predictive biomarkers for prognosis of epithelial ovarian cancer. Diagn. Pathol. 9, 178 (2014)CrossRefPubMedPubMedCentral W.N. Wan, Y.Q. Zhang, X.M. Wang, Y.J. Liu, Y.X. Zhang, Y.H. Que, W.J. Zhao, P. Li, Down-regulated miR-22 as predictive biomarkers for prognosis of epithelial ovarian cancer. Diagn. Pathol. 9, 178 (2014)CrossRefPubMedPubMedCentral
50.
Zurück zum Zitat L. Poliseno, L. Salmena, L. Riccardi, A. Fornari, M.S. Song, R.M. Hobbs, P. Sportoletti, S. Varmeh, A. Egia, G. Fedele, L. Rameh, M. Loda, P.P. Pandolfi, Identification of the miR-106b ~ 25 microRNA cluster as a proto-oncogenic PTEN targeting intron that cooperates with its host gene MCM7 in transformation. Sci. Signal. 3, ra29 (2010)CrossRefPubMedPubMedCentral L. Poliseno, L. Salmena, L. Riccardi, A. Fornari, M.S. Song, R.M. Hobbs, P. Sportoletti, S. Varmeh, A. Egia, G. Fedele, L. Rameh, M. Loda, P.P. Pandolfi, Identification of the miR-106b ~ 25 microRNA cluster as a proto-oncogenic PTEN targeting intron that cooperates with its host gene MCM7 in transformation. Sci. Signal. 3, ra29 (2010)CrossRefPubMedPubMedCentral
51.
Zurück zum Zitat W. Wang, F. Li, Y. Zhang, Y. Tu, Q. Yang, X. Gao, Reduced expression of miR-22 in gastric cancer is related to clinicopathologic characteristics or patient prognosis. Diagn. Pathol. 8, 102 (2013)CrossRefPubMedPubMedCentral W. Wang, F. Li, Y. Zhang, Y. Tu, Q. Yang, X. Gao, Reduced expression of miR-22 in gastric cancer is related to clinicopathologic characteristics or patient prognosis. Diagn. Pathol. 8, 102 (2013)CrossRefPubMedPubMedCentral
52.
Zurück zum Zitat L. Zhou, J. He, Y. Zhang, MicroRNA-22 expression in hepatocellular carcinoma and its correlation with ezrin protein. J. Int. Med. Res. 41, 1009–1016 (2013)CrossRefPubMed L. Zhou, J. He, Y. Zhang, MicroRNA-22 expression in hepatocellular carcinoma and its correlation with ezrin protein. J. Int. Med. Res. 41, 1009–1016 (2013)CrossRefPubMed
54.
Zurück zum Zitat M.E. McLaughlin-Drubin, C.P. Crum, K. Munger, Human papillomavirus E7 oncoprotein induces KDM6A and KDM6B histone demethylase expression and causes epigenetic reprogramming. Proc. Natl. Acad. Sci. U. S. A. 108, 2130–2135 (2011)CrossRefPubMedPubMedCentral M.E. McLaughlin-Drubin, C.P. Crum, K. Munger, Human papillomavirus E7 oncoprotein induces KDM6A and KDM6B histone demethylase expression and causes epigenetic reprogramming. Proc. Natl. Acad. Sci. U. S. A. 108, 2130–2135 (2011)CrossRefPubMedPubMedCentral
55.
Zurück zum Zitat V. Kumar, H.J. Westra, J. Karjalainen, D.V. Zhernakova, T. Esko, B. Hrdlickova, R. Almeida, A. Zhernakova, E. Reinmaa, U. Võsa, M.H. Hofker, R.S. Fehrmann, J. Fu, S. Withoff, A. Metspalu, L. Franke, C. Wijmenga, Human disease-associated genetic variation impacts large intergenic non-coding RNA expression. PLoS Genet. 9, e1003201 (2013)CrossRefPubMedPubMedCentral V. Kumar, H.J. Westra, J. Karjalainen, D.V. Zhernakova, T. Esko, B. Hrdlickova, R. Almeida, A. Zhernakova, E. Reinmaa, U. Võsa, M.H. Hofker, R.S. Fehrmann, J. Fu, S. Withoff, A. Metspalu, L. Franke, C. Wijmenga, Human disease-associated genetic variation impacts large intergenic non-coding RNA expression. PLoS Genet. 9, e1003201 (2013)CrossRefPubMedPubMedCentral
56.
Zurück zum Zitat Y.W. Wang, H.S. Chang, C.H. Lin, W.C. Yu, HPV-18 E7 conjugates to c-Myc and mediates its transcriptional activity. Int. J. Biochem. Cell Biol. 39, 402–412 (2007)CrossRefPubMed Y.W. Wang, H.S. Chang, C.H. Lin, W.C. Yu, HPV-18 E7 conjugates to c-Myc and mediates its transcriptional activity. Int. J. Biochem. Cell Biol. 39, 402–412 (2007)CrossRefPubMed
57.
Zurück zum Zitat T.C. Chang, D. Yu, Y.S. Lee, E.A. Wentzel, D.E. Arking, K.M. West, C.V. Dang, A. Thomas-Tikhonenko, J.T. Mendell, Widespread microRNA repression by Myc contributes to tumorigenesis. Nat. Genet. 40, 43–50 (2008)CrossRefPubMed T.C. Chang, D. Yu, Y.S. Lee, E.A. Wentzel, D.E. Arking, K.M. West, C.V. Dang, A. Thomas-Tikhonenko, J.T. Mendell, Widespread microRNA repression by Myc contributes to tumorigenesis. Nat. Genet. 40, 43–50 (2008)CrossRefPubMed
58.
Zurück zum Zitat J. Xiong, Q. Du, Z. Liang, Tumor-suppressive microRNA-22 inhibits the transcription of E-box-containing c-Myc target genes by silencing c-Myc binding protein. Oncogene 29, 4980–4988 (2010)CrossRefPubMed J. Xiong, Q. Du, Z. Liang, Tumor-suppressive microRNA-22 inhibits the transcription of E-box-containing c-Myc target genes by silencing c-Myc binding protein. Oncogene 29, 4980–4988 (2010)CrossRefPubMed
59.
Zurück zum Zitat M.Z. Ma, C.X. Li, Y. Zhang, M.Z. Weng, M.D. Zhang, Y.Y. Qin, W. Gong, Z.W. Quan, Long non-coding RNA HOTAIR, a c-Myc activated driver of malignancy, negatively regulates miRNA-130a in gallbladder cancer. Mol. Cancer 13, 156 (2014)CrossRefPubMedPubMedCentral M.Z. Ma, C.X. Li, Y. Zhang, M.Z. Weng, M.D. Zhang, Y.Y. Qin, W. Gong, Z.W. Quan, Long non-coding RNA HOTAIR, a c-Myc activated driver of malignancy, negatively regulates miRNA-130a in gallbladder cancer. Mol. Cancer 13, 156 (2014)CrossRefPubMedPubMedCentral
60.
Zurück zum Zitat T. Chiyomaru, S. Yamamura, S. Fukuhara, H. Yoshino, T. Kinoshita, S. Majid, S. Saini, I. Chang, Y. Tanaka, H. Enokida, N. Seki, M. Nakagawa, R. Dahiya, Genistein inhibits prostate cancer cell growth by targeting miR-34a and oncogenic HOTAIR. PLoS One 8, e70372 (2013)CrossRefPubMedPubMedCentral T. Chiyomaru, S. Yamamura, S. Fukuhara, H. Yoshino, T. Kinoshita, S. Majid, S. Saini, I. Chang, Y. Tanaka, H. Enokida, N. Seki, M. Nakagawa, R. Dahiya, Genistein inhibits prostate cancer cell growth by targeting miR-34a and oncogenic HOTAIR. PLoS One 8, e70372 (2013)CrossRefPubMedPubMedCentral
61.
Zurück zum Zitat X. Wang, H.-K. Wang, L. Yang, M. Hafner, N.S. Banerjee, S. Tang, D. Briskin, C. Meyers, L.T. Chow, X. Xie, T. Tuschl, Z.M. Zheng, microRNAs are biomarkers of oncogenic human papillomavirus infections. Proc. Natl. Acad. Sci. U. S. A. 111, 4262–4267 (2014)CrossRefPubMedPubMedCentral X. Wang, H.-K. Wang, L. Yang, M. Hafner, N.S. Banerjee, S. Tang, D. Briskin, C. Meyers, L.T. Chow, X. Xie, T. Tuschl, Z.M. Zheng, microRNAs are biomarkers of oncogenic human papillomavirus infections. Proc. Natl. Acad. Sci. U. S. A. 111, 4262–4267 (2014)CrossRefPubMedPubMedCentral
62.
Zurück zum Zitat B. Li, Y. Hu, F. Ye, Y. Li, W. Lv, X. Xie, Reduced miR 34a expression in normal cervical tissues and cervical lesions with high-risk human papillomavirus infection. Int. J. Gynecol. Cancer 20, 597–604 (2010)CrossRefPubMed B. Li, Y. Hu, F. Ye, Y. Li, W. Lv, X. Xie, Reduced miR 34a expression in normal cervical tissues and cervical lesions with high-risk human papillomavirus infection. Int. J. Gynecol. Cancer 20, 597–604 (2010)CrossRefPubMed
63.
Zurück zum Zitat X. Wang, H.K. Wang, J.P. McCoy, N.S. Banerjee, J.S. Rader, T.R. Broker, C. Meyers, L.T. Chow, Z.M. Zheng, Oncogenic HPV infection interrupts the expression of tumor-suppressive miR-34a through viral oncoprotein E6. RNA 15, 637–647 (2009)CrossRefPubMedPubMedCentral X. Wang, H.K. Wang, J.P. McCoy, N.S. Banerjee, J.S. Rader, T.R. Broker, C. Meyers, L.T. Chow, Z.M. Zheng, Oncogenic HPV infection interrupts the expression of tumor-suppressive miR-34a through viral oncoprotein E6. RNA 15, 637–647 (2009)CrossRefPubMedPubMedCentral
Metadaten
Titel
Identification of genetic variation in the lncRNA HOTAIR associated with HPV16-related cervical cancer pathogenesis
verfasst von
Sweta Sharma Saha
Rahul Roy Chowdhury
Nidhu Ranjan Mondal
Biman Chakravarty
Tanmay Chatterjee
Sudipta Roy
Sharmila Sengupta
Publikationsdatum
28.09.2016
Verlag
Springer Netherlands
Erschienen in
Cellular Oncology / Ausgabe 6/2016
Print ISSN: 2211-3428
Elektronische ISSN: 2211-3436
DOI
https://doi.org/10.1007/s13402-016-0298-0

Weitere Artikel der Ausgabe 6/2016

Cellular Oncology 6/2016 Zur Ausgabe

Neu im Fachgebiet Pathologie