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

Cellular Oncology

Volumn 39, Issue 6, 2016, Pages 559-572

  Sharma Saha, Sweta ^a   Roy Chowdhury, Rahul ^b   Mondal, Nidhu Ranjan ^b   Chakravarty, Biman ^b   Chatterjee, Tanmay ^b   Roy, Sudipta ^c   Sengupta, Sharmila ^a  

^a NATIONAL INSTITUTE OF BIOMEDICAL GENOMICS   (India)

^b Saroj Gupta Cancer Centre and Research Institute   (India)

^c Sri Aurobindo Seva Kendra   (India)

Author keywords

Cervical cancer; HOTAIR; HPV16 E7; lncRNA; SNP

Indexed keywords

GENOMIC DNA; LONG UNTRANSLATED RNA; MICRORNA; MICRORNA 22; PROTEIN E7; TUMOR MARKER; HOTAIR LONG UNTRANSLATED RNA, HUMAN;

ADULT; AGED; AMPLICON; ARTICLE; BINDING SITE; CONTROLLED STUDY; DOWN REGULATION; FEMALE; GENE OVEREXPRESSION; GENETIC ASSOCIATION; GENETIC VARIATION; HISTOPATHOLOGY; HOTAIR GENE; HUMAN; HUMAN PAPILLOMAVIRUS TYPE 16; HUMAN TISSUE; LUCIFERASE ASSAY; NONHUMAN; ONCOGENE; PATHOGENESIS; PLASMID; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; UTERINE CERVIX CANCER; COMPLICATION; GENETICS; MIDDLE AGED; PAPILLOMAVIRUS INFECTION; PATHOLOGY; SINGLE NUCLEOTIDE POLYMORPHISM; SQUAMOUS CELL CARCINOMA; UTERINE CERVIX TUMOR; VIROLOGY;

ADULT; AGED; CARCINOMA, SQUAMOUS CELL; DOWN-REGULATION; FEMALE; HUMAN PAPILLOMAVIRUS 16; HUMANS; MIDDLE AGED; PAPILLOMAVIRUS INFECTIONS; POLYMORPHISM, SINGLE NUCLEOTIDE; REAL-TIME POLYMERASE CHAIN REACTION; RNA, LONG NONCODING; UTERINE CERVICAL NEOPLASMS;

EID: 84988951273     PISSN: 22113428     EISSN: 22113436     Source Type: Journal    
DOI: 10.1007/s13402-016-0298-0     Document Type: Article

References (63)

1. 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. Guidelines for cervical cancer screening programme. Government of India - World Health Organization Collaboration Programme 2004–2005 (2006)
3. H. zur Hausen, Papillomavirus infections–a major cause of human cancers. Biochim. Biophys. Acta 1288, F55–F78 (1996)
4. 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)
5. 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)
6. 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)
7. 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)
8. 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)
9. 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)
10. 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)
11. 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)
12. C.P. Ponting, P.L. Oliver, W. Reik, Evolution and functions of long noncoding RNAs. Cell 136, 629–641 (2009)
13. K.C. Wang, H.Y. Chang, Molecular mechanisms of long noncoding RNAs. Mol. Cell 43, 904–914 (2011)
14. M. Vitiello, A. Tuccoli, L. Poliseno, Long non-coding RNAs in cancer: implications for personalized therapy. Cell. Oncol. 38, 17–28 (2015)
15. 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)
16. 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)
17. 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)
18. T. Nagano, P. Fraser, No-nonsense functions for long noncoding RNAs. Cell 145, 178–181 (2011)
19. V. Taucher, H. Mangge, J. Haybaeck, Non-coding RNAs in pancreatic cancer: challenges and opportunities for clinical application. Cell. Oncol. 39, 295–318 (2016)
20. M. Huarte, J.L. Rinn, Large non-coding RNAs: missing links in cancer? Hum. Mol. Genet. 19, R152–R161 (2010)
21. 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)
22. 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)
23. A. Ferraro, Altered primary chromatin structures and their implications in cancer development. Cell. Oncol. 39, 195–210 (2016)
24. 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)
25. 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)
26. 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)
27. 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)
28. 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)
29. 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)
30. 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)
31. 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)
32. 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)
33. 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)
34. 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)
35. 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)
36. 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)
37. 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)
38. 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)
39. 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)
40. 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)
41. 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)
42. 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)
43. 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)
44. 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)
45. 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)
46. 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)
47. 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)
48. 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)
49. 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)
50. 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)
51. 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)
52. 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)
53. K. Dimopoulos, P. Gimsing, K. Grønbæk, The role of epigenetics in the biology of multiple myeloma. Blood Cancer J. 4, e207 (2014)
54. 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)
55. 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)
56. 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)
57. 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)
58. 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)
59. 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)
60. 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)
61. 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)
62. 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)
63. 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)