The role of HPV‑induced epigenetic changes in cervical carcinogenesis (Review)
- Authors:
- Martha Laysla Ramos Da Silva
- Beatriz Helena Dantas Rodrigues De Albuquerque
- Thales Araújo De Medeiros Fernandes Allyrio
- Valéria Duarte De Almeida
- Ricardo Ney De Oliveira Cobucci
- Fabiana Lima Bezerra
- Vania Sousa Andrade
- Daniel Carlos Ferreira Lanza
- Jenner Christian Veríssimo De Azevedo
- Josélio Maria Galvão De Araújo
- José Veríssimo Fernandes
-
Affiliations: Department of Microbiology and Parasitology, Federal University of Rio Grande do Norte, Natal 59078‑970, Brazil, Laboratory of Applied Molecular Biology, Department of Biochemistry, Federal University of Rio Grande do Norte, Natal 59078‑970, Brazil, Department of Biomedical Sciences, State University of Rio Grande do Norte, Mossoro 59607‑360, Brazil, Department of Gynecology and Obstetrics, Potiguar University, Natal 59056‑000, Brazil, Department of Pediatrics, Federal University of Rio Grande do Norte, Natal 59012‑570, Brazil - Published online on: May 20, 2021 https://doi.org/10.3892/br.2021.1436
- Article Number: 60
-
Copyright: © Da Silva et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
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|
Liang J, Zhang S, Wang W, Xu Y, Kawuli A, Lu J and Xiu X: Long non-coding RNA DSCAM-AS1 contributes to the tumorigenesis of cervical cancer by targeting miR-877-5p/ATXN7L3 axis. Biosci Rep. 40(BSR20192061)2020.PubMed/NCBI View Article : Google Scholar | |
|
Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D and Bray F: Cancer incidence and mortality worldwide: Sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 136:E359–E386. 2015.PubMed/NCBI View Article : Google Scholar | |
|
Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J and Jemal A: Global cancer statistics, 2012. CA Cancer J Clin. 65:87–108. 2015.PubMed/NCBI View Article : Google Scholar | |
|
INCA: Estimativa 2018: Incidência de câncer no Brasil/Instituto Nacional de Câncer Jose Alencar Gomes da Silva. Coordenação de Prevenção e Vigilância, Rio de Janeiro, 2017. | |
|
Chen L, Qiu X, Zhang N, Wang Y, Wang M, Li D, Wang L and Du Y: APOBEC-mediated genomic alterations link immunity and viral infection during human papillomavirus-driven cervical carcinogenesis. Biosci Trends. 11:383–388. 2017.PubMed/NCBI View Article : Google Scholar | |
|
Sen P, Ganguly P and Ganguly N: Modulation of DNA methylation by human papillomavirus E6 and E7 oncoproteins in cervical cancer. Oncol Lett. 15:11–22. 2018.PubMed/NCBI View Article : Google Scholar | |
|
Senapati R, Senapati NN and Dwibedi B: Molecular mechanisms of HPV mediated neoplastic progression. Infect Agent Cancer. 11(59)2016.PubMed/NCBI View Article : Google Scholar | |
|
Steenbergen RD, Snijders PJ, Heideman DA and Meijer CJ: Clinical implications of (epi)genetic changes in HPV-induced cervical precancerous lesions. Nat Rev Cancer. 14:395–405. 2014.PubMed/NCBI View Article : Google Scholar | |
|
Morel A, Baguet A, Perrard J, Demeret C, Jacquin E, Guenat D, Mougin C and Prétet JL: 5azadC treatment upregulates miR-375 level and represses HPV16 E6 expression. Oncotarget. 8:46163–46176. 2017.PubMed/NCBI View Article : Google Scholar | |
|
Fernandes JV, de Medeiros Fernandes TA, de Azevedo JC, Cobucci RN, de Carvalho MG, Andrade VS and de Araújo JM: Link between chronic inflammation and human papillomavirus-induced carcinogenesis (Review). Oncol Lett. 9:1015–1026. 2015.PubMed/NCBI View Article : Google Scholar | |
|
Soto D, Song C and McLaughlin-Drubin ME: Epigenetic alterations in human papillomavirus-associated cancers. Viruses. 9(248)2017.PubMed/NCBI View Article : Google Scholar | |
|
Durzynska J, Lesniewicz K and Poreba E: Human papillomaviruses in epigenetic regulations. Mutat Res Rev Mutat Res. 772:36–50. 2017.PubMed/NCBI View Article : Google Scholar | |
|
Amaro-Filho SM, Pereira Chaves CB, Felix SP, Basto DL, de Almeida LM and Moreira MAM: HPV DNA methylation at the early promoter and E1/E2 integrity: A comparison between HPV16, HPV18 and HPV45 in cervical cancer. Papillomavirus Res. 5:172–179. 2018.PubMed/NCBI View Article : Google Scholar | |
|
Jacquin E, Baraquin A, Ramanah R, Carcopino X, Morel A, Valmary-Degano S, Bravo IG, de Sanjosé S, Riethmuller D, Mougin C and Prétet JL: Methylation of human papillomavirus type 16 CpG sites at E2-binding site 1 (E2BS1), E2BS2, and the Sp1-binding site in cervical cancer samples as determined by high-resolution melting analysis-PCR. J Clin Microbiol. 51:3207–3215. 2013.PubMed/NCBI View Article : Google Scholar | |
|
Loscalzo J and Handy DE: Epigenetic modifications: Basic mechanisms and role in cardiovascular disease (2013 Grover Conference series). Pulm Circ. 4:169–174. 2014.PubMed/NCBI View Article : Google Scholar | |
|
Shamsi MB, Firoz AS, Imam SN, Alzaman N and Samman MA: Epigenetics of human diseases and scope in future therapeutics. J Taibah Univ Med Sci. 212:205–211. 2017.PubMed/NCBI View Article : Google Scholar | |
|
Vogt G: Facilitation of environmental adaptation and evolution by epigenetic phenotype variation: Insights from clonal, invasive, polyploid, and domesticated animals. Environ Epigenet. 3(dvx002)2017.PubMed/NCBI View Article : Google Scholar | |
|
Marsit CJ: Influence of environmental exposure on human epigenetic regulation. J Exp Biology. 218:71–79. 2015.PubMed/NCBI View Article : Google Scholar | |
|
Li Y and Tollefsbol TO: Age-related epigenetic drift and phenotypic plasticity loss: Implications in prevention of age-related human diseases. Epigenomics. 8:1637–1651. 2016.PubMed/NCBI View Article : Google Scholar | |
|
Zannas AS and Chrousos GP: Epigenetic programming by stress and glucocorticoids along the human lifespan. Mol Psychiatry. 22:640–646. 2017.PubMed/NCBI View Article : Google Scholar | |
|
Osborne A: The role of epigenetics in human evolution. Biosc Horizons. 10(hzx007)2017. | |
|
Stefansson OA and Esteller M: Epigenetic modifications in breast cancer and their role in personalized medicine. Am J Pathol. 183:1052–1063. 2013.PubMed/NCBI View Article : Google Scholar | |
|
Llinàs-Arias P and Esteller M: Epigenetic inactivation of tumor suppressor coding and non-coding genes in human cancer: An update. Open Biol. 7(170152)2017.PubMed/NCBI View Article : Google Scholar | |
|
Ramassone A, Pagotto S, Veronese A and Visone R: Epigenetics and microRNAs in cancer. Int J Mol Sci. 19(459)2018.PubMed/NCBI View Article : Google Scholar | |
|
Kurdyukov S and Bullock M: DNA methylation analysis: Choosing the right method. Biology (Basel). 5(3)2016.PubMed/NCBI View Article : Google Scholar | |
|
Zhang X, Hu M, Lyu X, Li C, Thannickal VJ and Sanders YY: DNA methylation regulated gene expression in organ fibrosis. Biochim Biophys Acta Mol Basis Dis. 1863:2389–2397. 2017.PubMed/NCBI View Article : Google Scholar | |
|
Yang X, Han H, de Carvalho DD, Lay FD, Jones PA and Liang G: Gene body methylation can alter gene expression and is a therapeutic target in cancer. Cancer Cell. 26:577–590. 2014.PubMed/NCBI View Article : Google Scholar | |
|
Jin Z and Liu Y: DNA methylation in human diseases. Genes Dis. 5:1–8. 2018.PubMed/NCBI View Article : Google Scholar | |
|
Moore LD, Le T and Fan G: DNA Methylation and its basic function. Neuropsychopharmacology. 38:23–38. 2013.PubMed/NCBI View Article : Google Scholar | |
|
Ehrlich M: DNA hypomethylation in cancer cells. Epigenomics. 1:239–259. 2009.PubMed/NCBI View Article : Google Scholar | |
|
Yang HJ: Aberrant DNA methylation in cervical carcinogenesis. Chin J Cancer. 32:42–48. 2013.PubMed/NCBI View Article : Google Scholar | |
|
Lu Q, Ma D and Zhao S: DNA methylation changes in cervical cancers. Methods Mol Biol. 863:155–176. 2012.PubMed/NCBI View Article : Google Scholar | |
|
Liu G: CDH1 promoter methylation in patients with cervical carcinoma: A systematic meta-analysis with trial sequential analysis. Future Oncol. 14:51–63. 2018.PubMed/NCBI View Article : Google Scholar | |
|
Snoek BC, Splunter AP, Bleeker MC, Ruiten MC, Heideman DA, Rurup WF, Verlaat W, Schotman H, Gent MV, Trommel NE and Steenbergen RD: Cervical cancer detection by DNA methylation analysis in urine. Sci Rep. 9(3088)2019.PubMed/NCBI View Article : Google Scholar | |
|
McCormick TM, Canedo NH, Furtado YL, Silveira FA, de Lima RJ, Rosman AD, Almeida Filho GL and Carvalho Mda G: Association between human papillomavirus and Epstein-Barr virus DNA and gene promoter methylation of RB1 and CDH1 in the cervical lesions: A transversal study. Diagn Pathol. 10(59)2015.PubMed/NCBI View Article : Google Scholar | |
|
Cardoso MF, Castelletti CH, Lima-Filho JL, Martins DB and Teixeira JA: Putative biomarkers for cervical cancer: SNVs, methylation and expression profiles. Mutat Res. 773:161–173. 2017.PubMed/NCBI View Article : Google Scholar | |
|
Fernandes JV, Araújo JM and Fernandes TA: Biology and natural history of human papillomavirus infection. Open Access J Clin Trials. 2013(5)2013. | |
|
Bashaw AA, Leggatt GR, Chandra J, Tuong ZK and Frazer IH: Modulation of antigen presenting cell functions during chronic HPV infection. Papillomavirus Res. 4:58–65. 2017.PubMed/NCBI View Article : Google Scholar | |
|
Yang M, Wang M, Li X, Xie Y, Xia X, Tian J, Zhang K and Tang A: Wnt signaling in cervical cancer? J Cancer. 9:1277–1286. 2018.PubMed/NCBI View Article : Google Scholar | |
|
Ayala-Calvillo A, Mojica-Vázquer LH, García-Carrancá A and González-Maya L: Wnt/β-catenin pathway activation and silencing of the APC gene in HPV-positive human cervical cancer-derived cells. Mol Med Rep. 17:200–208. 2018.PubMed/NCBI View Article : Google Scholar | |
|
Lee J and Kim SS: The function of p27 KIP1 during tumor development. Exp Mol Med. 41:765–771. 2009.PubMed/NCBI View Article : Google Scholar | |
|
Qi Q, Ling Y, Zhu M, Zhou L, Wan M, Bao Y and Liu Y: Promoter region methylation and loss of protein expression of PTEN and significance in cervical cancer. Biomed Rep. 2:653–658. 2014.PubMed/NCBI View Article : Google Scholar | |
|
Li JY, Huang T, Zhang C, Jiang DJ, Hong QX, Ji HH, Ye M and Duan SW: Association between RASSF1A promoter hypermethylation and oncogenic HPV infection status in invasive cervical cancer: A meta-analysis. Asian Pac J Cancer Prev. 16:5749–754. 2015.PubMed/NCBI View Article : Google Scholar | |
|
Sherr CJ and Bartek J: Cell cycle-targeted cancer therapies. Ann Rev Cancer Biol. 1:41–57. 2017. | |
|
Li X, Tao L, Tan Q, Dong Y, Pan X, Pang L, Qi Y, Zou H, Liang W, Liu W, et al: CpG island methylation of the CADM1 gene correlates with cervical carcinogenesis in the Uighur and Han populations of Xinjiang, China. Int J Clin Exp Pathol. 9:6977–6987. 2016. | |
|
Holubeková V, Mendelová A, Grendár M, Meršaková S, Kapustová I, Jašek K, Vaňochová A, Danko J and Lasabová Z: Methylation pattern of CDH1 promoter and its association with CDH1 gene expression in cytological cervical specimens. Oncol Lett. 12:2613–2621. 2016.PubMed/NCBI View Article : Google Scholar | |
|
Siegel EM, Riggs BM, Delmas AL, Koch A, Hakam A and Brown KD: Quantitative DNA methylation analysis of candidate genes in cervical cancer. PLoS One. 10(e0122495)2015.PubMed/NCBI View Article : Google Scholar | |
|
Lorincz AT: Virtues and weaknesses of DNA methylation as a test for cervical cancer prevention. Acta Cytol. 60:501–512. 2016.PubMed/NCBI View Article : Google Scholar | |
|
Kim MK, Lee IH, Lee KH, Lee YK, So KA, Hong SR, Hwang CS, Kee MK, Rhee JE, Kang C, et al: DNA methylation in human papillomavirus-infected cervical cells is elevated in high-grade squamous intraepithelial lesions and cancer. J Gynecol Oncol. 27(e14)2016.PubMed/NCBI View Article : Google Scholar | |
|
Chang CC, Huang RL, Wang HC, Liao YP, Yu MH and Lai HC: High methylation rate of LMX1A, NKX6-1, PAX1, PTPRR, SOX1, and ZNF582 genes in cervical adenocarcinoma. Int J Gynecol Cancer. 24:201–209. 2014.PubMed/NCBI View Article : Google Scholar | |
|
Xu L, Xu J, Hu Z, Yang B, Wang L, Lin X, Xia Z, Zhang Z and Zhu Y: Quantitative DNA methylation analysis of paired box gene 1 and LIM homeobox transcription factor 1α genes in cervical cancer. Oncol Lett. 15:4477–4484. 2018.PubMed/NCBI View Article : Google Scholar | |
|
Flamini MI, Gauna GV, Sottile ML, Nadin BS, Sanchez AM and Vargas-Roig LM: Retinoic acid reduces migration of human breast cancer cells: Role of retinoic acid receptor beta. J Cell Mol Med. 18:1113–1123. 2014.PubMed/NCBI View Article : Google Scholar | |
|
Yin FF, Wang N, Bi XN, Yu X, Xu XH, Wang YL, Zhao CQ, Luo B and Wang YK: Serine/threonine kinases 31(STK31) may be a novel cellular target gene for the HPV16 oncogene E7 with potential as a DNA hypomethylation biomarker in cervical cancer. Virol J. 13(60)2016.PubMed/NCBI View Article : Google Scholar | |
|
Molano M, Moreno-Acosta P, Morales N, Burgos M, Buitrago L, Gamboa O, Alvarez R, Garland SM, Tabrizi SN, Steenbergen RD and Mejía JC: Association between type-specific HPV infections and hTERT DNA methylation in patients with invasive cervical cancer. Cancer Genomics Proteomics. 13:483–491. 2016.PubMed/NCBI View Article : Google Scholar | |
|
Johannsen E and Lambert PF: Epigenetics of human papillomaviruses. Virology. 445:205–212. 2013.PubMed/NCBI View Article : Google Scholar | |
|
Simanaviciene V, Popendikyte V, Gudleviciene Z and Zvirbliene A: Different DNA methylation pattern of HPV16, HPV18 and HPV51 genomes in asymptomatic HPV infection as compared to cervical neoplasia. Virology. 484:227–233. 2015.PubMed/NCBI View Article : Google Scholar | |
|
Wang W, Sun Z, Liu J, Wang G, Lu Z, Zhou W, Qi T and Ruan Q: Increased methylation of human papillomavirus type 16 DNA is associated with the severity of cervical lesions in infected females from northeast China. Oncol Lett. 13:3809–3816. 2017.PubMed/NCBI View Article : Google Scholar | |
|
McBride AA and Warburton A: The role of integration in oncogenic progression of HPV-associated cancers. PLoS Pathog. 13(e1006211)2017.PubMed/NCBI View Article : Google Scholar | |
|
Vinokurova S and von Knebel Doeberitz M: Differential methylation of the HPV 16 upstream regulatory region during epithelial differentiation and neoplastic transformation. PLoS One. 6(e24451)2011.PubMed/NCBI View Article : Google Scholar | |
|
McBride AA: The papillomavirus E2 proteins. Virology. 445:57–79. 2013.PubMed/NCBI View Article : Google Scholar | |
|
Filho SM, Bertoni N, Brant AC, Vidal JP, Felix SP, Cavalcanti SM, Carestiato FN, Martins LF, Almeida LM and Moreira MA: Methylation at 3'LCR of HPV16 can be affected by patient age and disruption of E1 or E2 genes. Virus Res. 232:48–53. 2017.PubMed/NCBI View Article : Google Scholar | |
|
Fertey J, Hagmann J, Ruscheweyh HJ, Munk C, Kjaer S, Huson D, Haedicke-Jarboui J, Stubenrauch F and Iftner T: Methylation of CpG 5962 in L1 of the human papillomavirus 16 genome as a potential predictive marker for viral persistence: A prospective large cohort study using cervical swab samples. Cancer Med. 9:1058–1068. 2019.PubMed/NCBI View Article : Google Scholar | |
|
Niyazi M, Sui S, Zhu K, Wang L, Jiao Z and Lu P: Correlation between methylation of human papillomavirus-16 L1 gene and cervical carcinoma in Uyghur women. Gynecol Obstet Invest. 82:22–29. 2017.PubMed/NCBI View Article : Google Scholar | |
|
Huang J, Tan ZR, Yu J, Li H, Lv QL, Shao YY and Zhou HH: DNA hypermethylated status and gene expression of PAX1/SOX1 in patients with colorectal carcinoma. Onco Targets Ther. 10:4739–4751. 2017.PubMed/NCBI View Article : Google Scholar | |
|
Luan T, Hua Q, Liu X, Xu P, Gu Y, Qian H, Yan L, Xu X, Geng R, Zeng X and Li P: PAX1 Methylation as a potential biomarker to predict the progression of cervical intraepithelial neoplasia: A Meta-analysis of related studies. Int J Gynecol Cancer. 27:1480–1488. 2017.PubMed/NCBI View Article : Google Scholar | |
|
Lin YW, Tsao CM, Yu PN, Shih YL, Lin CH and Yan MD: SOX1 suppresses cell growth and invasion in cervical cancer. Gynecol Oncol. 131:174–181. 2013.PubMed/NCBI View Article : Google Scholar | |
|
Bowden SJ, Kalliala I, Veroniki AA, Arbyn M, Mitra A, Lathouras K, Mirabello L, Chadeau-Hyam M, Paraskevaidis E, Flanagan JM and Kyrgiou M: The use of human papillomavirus DNA methylation in cervical intraepithelial neoplasia: A systematic review and meta-analysis. EBioMedicine. 50:246–59. 2019.PubMed/NCBI View Article : Google Scholar | |
|
Torres-Rojas FI, Alarcón-Romero LC, Leyva-Vázquez MA, Ortiz-Ortiz J, Mendoza-Catalán MÁ, Hernández-Sotelo D, Moral-Hernández OD, Rodríguez-Ruiz HA, Leyva-Illades D, Flores-Alfaro E and Illades-Aguiar B: Methylation of the L1 gene and integration of human papillomavirus 16 and 18 in cervical carcinoma and premalignant lesions. Oncol Lett. 15:2278–2286. 2018.PubMed/NCBI View Article : Google Scholar | |
|
Clarke MA, Gradissimo A, Schiffman M, Lam J, Sollecito CC, Fetterman B, Lorey T, Poitras N, Raine-Bennett TR, Castle PE, et al: Human papillomavirus DNA methylation as a biomarker for cervical precancer: Consistency across 12 genotypes and potential impact on management of HPV-positive women. Clin Cancer Res. 24:2194–2202. 2018.PubMed/NCBI View Article : Google Scholar | |
|
Shestakova EA and Nakatani Y: Characterization of histone predeposition complexes from different cellular compartments. J Investig Genomics. 2:25–28. 2015. | |
|
Bornelöv S, Reynolds N, Xenophontos M, Gharbi S, Johnstone E, Floyd R, Ralser M, Signolet J, Loos R, Dietmann S, et al: The nucleosome remodeling and deacetylation complex modulates chromatin structure at sites of active transcription to fine-tune gene expression. Mol Cell. 71:56–72.e4. 2018.PubMed/NCBI View Article : Google Scholar | |
|
Feng T, Wang H, Su H, Lu H, Yu L, Zhang X, Sun H and You Q: Novel N-hydroxyfurylacrylamide-based histone deacetylase (HDAC) inhibitors with branched CAP group (Part 2). Bioorg Med Chem. 21:5339–5354. 2013.PubMed/NCBI View Article : Google Scholar | |
|
Li B, Carey M and Workman JL: The role of chromatin during transcription. Cell. 128:707–719. 2007.PubMed/NCBI View Article : Google Scholar | |
|
Zhang H, Dai X, Qi Y, He Y, Du W and Pang JJ: Histone deacetylases inhibitors in the treatment of retinal degenerative diseases: Overview and perspectives. J Ophthalmol. 2015(250812)2015.PubMed/NCBI View Article : Google Scholar | |
|
Song C, Zhu S, Wu C and Kang J: Histone deacetylase (HDAC) 10 suppresses cervical cancer metastasis through inhibition of matrix metalloproteinase (MMP) 2 and 9 expression. J Biol Chem. 288:28021–2833. 2013.PubMed/NCBI View Article : Google Scholar | |
|
Kondo Y, Shen L, Cheng AS, Ahmed S, Boumber Y, Charo C, Yamochi T, Urano T, Furukawa K, Kwabi-Addo B, et al: Gene silencing in cancer by histone H3 lysine 27 trimethylation independent of promoter DNA methylation. Nat Genet. 40:741–750. 2008.PubMed/NCBI View Article : Google Scholar | |
|
Hiragami-Hamada K, Xie SQ, Saveliev A, Uribe-Lewis S, Pombo A and Festenstein R: The molecular basis for stability of heterochromatin-mediated silencing in mammals. Epigenetics Chromatin. 2(14)2009.PubMed/NCBI View Article : Google Scholar | |
|
Scarpini CG, Groves IJ, Pett MR, Ward D and Coleman N: Virus transcript levels and cell growth rates after naturally occurring HPV16 integration events in basal cervical keratinocytes. J Pathol. 233:281–293. 2014.PubMed/NCBI View Article : Google Scholar | |
|
Yeo-Teh NSL, Ito Y and Jha S: High-Risk human papillomaviral oncogenes E6 and E7 target key cellular pathways to achieve oncogenesis. Int J Mol Sci. 19(1706)2018.PubMed/NCBI View Article : Google Scholar | |
|
Uchida C: Roles of pRB in the regulation of nucleosome and chromatin structures. Biomed Res Int. 2016(5959721)2016.PubMed/NCBI View Article : Google Scholar | |
|
Fischer M: Census and evaluation of p53 target genes. Oncogene. 36:3943–3956. 2017.PubMed/NCBI View Article : Google Scholar | |
|
Zhang Y, Dakic A, Chen R, Dai Y, Schlegel R and Liu X: Direct HPV E6/Myc interactions induce histone modifications, Pol II phosphorylation, and hTERT promoter activation. Oncotarget. 8:96323–96339. 2017.PubMed/NCBI View Article : Google Scholar | |
|
Johansson C, Jamal Fattah T, Yu H, Nygren J, Mossberg AK and Schwartz S: Acetylation of intragenic histones on HPV16 correlates with enhanced HPV16 gene expression. Virology. 482:244–259. 2015.PubMed/NCBI View Article : Google Scholar | |
|
Zhang L, Yuan C, Wang Y and Zhao S: Histone deacetylases 3 (HDAC3) is highly expressed in cervical cancer and inhibited by siRNA. Int J Clin Exp Pathol. 9:3600–3605. 2016. | |
|
Chen X, Loo JX, Shi X, Xiong W, Guo Y, Ke H, Yang M, Jiang Y, Xia S, Zhao M, et al: E6 protein expressed by high-risk HPV activates super-enhancers of the EGFR and c-MET oncogenes by destabilizing the histone demethylase KDM5C. Cancer. 78:1418–1430. 2018.PubMed/NCBI View Article : Google Scholar | |
|
Wang WT, Han C, Sun YM, Chen TQ and Chen YQ: Noncoding RNAs in cancer therapy resistance and targeted drug development. J Hematol Oncol. 12(55)2019.PubMed/NCBI View Article : Google Scholar | |
|
Sadri Nahand J, Moghoofei M, Salmaninejad A, Bahmanpour Z, Karimzadeh M, Nasiri M, Mirzaei HR, Pourhanifeh MH, Bokharaei-Salim F, Mirzaei H and Hamblin MR: Pathogenic role of exosomes and microRNAs in HPV-mediated inflammation and cervical cancer: A review. Int J Cancer. 146:305–320. 2020.PubMed/NCBI View Article : Google Scholar | |
|
Łaniewski P, Cui H, Roe DJ, Barnes D, Goulder A, Monk BJ, Greenspan DL, Chase DM and Herbst-Kralovetz MM: Features of the cervicovaginal microenvironment drive cancer biomarker signatures in patients across cervical carcinogenesis. Sci Rep. 9(7333)2019.PubMed/NCBI View Article : Google Scholar | |
|
Gupta SM and Mania-Pramanik J: Retraction note: Molecular mechanisms in progression of HPV-associated cervical carcinogenesis. J Biomed Sci. 26(50)2019.PubMed/NCBI View Article : Google Scholar | |
|
Zheng ZM and Wang X: Regulation of cellular miRNA expression by human papillomaviruses. Biochim Biophys Acta. 26:668–677. 2011.PubMed/NCBI View Article : Google Scholar | |
|
Liu Z, Luo S, Wu M, Huang C, Shi H and Song X: LncRNA GHET1 promotes cervical cancer progression through regulating AKT/mTOR and Wnt/β-catenin signaling pathways. Biosci Rep. 40(BSR20191265)2020.PubMed/NCBI View Article : Google Scholar | |
|
Fouad YA and Aanei C: Revisiting the hallmarks of cancer. Am J Cancer Res. 7:1016–1036. 2017.PubMed/NCBI | |
|
Oliveto S, Mancino M, Manfrini N and Biffo S: Role of microRNAs in translation regulation and cancer. World J Biol Chem. 8:45–56. 2017.PubMed/NCBI View Article : Google Scholar | |
|
Zamani S, Sohrabi A, Hosseini SM, Rahnamaye-Farzami M and Akbari A: Deregulation of miR-21 and miR-29a in cervical cancer related to HPV infection. Microrna. 8:110–115. 2019.PubMed/NCBI View Article : Google Scholar | |
|
Vaschetto LM: miRNA activation is an endogenous gene expression pathway. RNA Biol. 156:826–828. 2018.PubMed/NCBI View Article : Google Scholar | |
|
Zhou K, Liu M and Cao Y: New insight into microRNA fnctions in cancer: Oncogene-microRNA-tumor suppressor gene network. Front Mol Biosci. 4(46)2017.PubMed/NCBI View Article : Google Scholar | |
|
Yeung CLA, Tsang TY, Yau PL and Kwok TT: Human papillomavirus type 16 E6 suppresses microRNA-23b expression in human cervical cancer cells through DNA methylation of the host gene C9orf3. Oncotarget. 8:12158–12173. 2017.PubMed/NCBI View Article : Google Scholar | |
|
Chen AH, Qin YE, Tang WF, Tao J, Song HM and Zuo M: miR-34a and miR-206 act as novel prognostic and therapy biomarkers in cervical cancer. Cancer Cell Int. 17(63)2017.PubMed/NCBI View Article : Google Scholar | |
|
Dong P, Xiong Y, Hanley SJB, Yue J and Watari H: Musashi-2, a novel oncoprotein promoting cervical cancer cell growth and invasion, is negatively regulated by p53-induced miR-143 and miR-107 activation. J Exp Clin Cancer Res. 36(150)2017.PubMed/NCBI View Article : Google Scholar | |
|
Ofir M, Hacohen D and Ginsberg D: miR-15 and miR-16 are direct transcriptional targets of E2F1 that limit E2F-induced proliferation by targeting cyclin E. Mol Cancer Res. 9:440–447. 2011.PubMed/NCBI View Article : Google Scholar | |
|
Chen X, Cao R, Liu H, Zhang T, Yuan X and Xu S: MicroRNA-15a-5p-targeting oncogene YAP1 inhibits cell viability and induces cell apoptosis in cervical cancer cells. Int J Mol Med. 46:1301–1310. 2020.PubMed/NCBI View Article : Google Scholar | |
|
Zhou M, Chen X, Wu J, He X and Ren R: MicroRNA-143 regulates cell migration and invasion by targeting GOLM1 in cervical cancer. Oncol Lett. 16:6393–6400. 2018.PubMed/NCBI View Article : Google Scholar | |
|
Sannigrahi MK, Sharma R, Singh V, Panda NK, Rattan V and Khullar M: Role of host miRNA Hsa-miR-139-3p in HPV-16-induced carcinomas. Clin Cancer Res. 23:3884–3895. 2017.PubMed/NCBI View Article : Google Scholar | |
|
Jiang Z, Song Q, Zeng R, Li J, Li J, Lin X, Chen X, Zhang J and Zheng Y: MicroRNA-218 inhibits EMT, migration and invasion by targeting SFMBT1 and DCUN1D1 in cervical cancer. Oncotarget. 7:45622–45636. 2016.PubMed/NCBI View Article : Google Scholar | |
|
Zhu L, Tu H, Liang Y and Tang D: miR-218 produces anti-tumor effects on cervical cancer cells in vitro. World J Surg Oncol. 16(204)2018.PubMed/NCBI View Article : Google Scholar | |
|
McLaughlin-Drubin ME and Münger K: The human papillomavirus E7 oncoprotein. Virology. 384:335–344. 2009.PubMed/NCBI View Article : Google Scholar | |
|
Myklebust MP, Bruland O, Fluge Ø, Skarstein A, Balteskard L and Dahl O: MicroRNA-15b is induced with E2F-controlled genes in HPV-related cancer. Br J Cancer. 105:1719–1725. 2011.PubMed/NCBI View Article : Google Scholar | |
|
Liu Z, Wu M, Shi H, Huang C, Luo S and Song X: DDN-AS1-miR-15a/16-TCF3 feedback loop regulates tumor progression in cervical cancer. J Cell Biochem. 120:10228–10238. 2019.PubMed/NCBI View Article : Google Scholar | |
|
Cheng Y, Geng L, Zhao L, Zuo P and Wang J: Human papillomavirus E6-regulated microRNA-20b promotes invasion in cervical cancer by targeting tissue inhibitor of metalloproteinase 2. Mol Med Rep. 16:5464–5470. 2017.PubMed/NCBI View Article : Google Scholar | |
|
Kong Q, Wang W and Li P: Regulator role of HPV E7 protein on miR-21 expression in cervical carcinoma cells and its functional implication. Int J Clin Exp Pathol. 8:15808–15813. 2015.PubMed/NCBI | |
|
Cai L, Wang W, Li X, Dong T, Zhang Q, Zhu B, Zhao H and Wu S: MicroRNA-21-5p induces the metastatic phenotype of human cervical carcinoma cells in vitro by targeting the von Hippel-Lindau tumor suppressor. Oncol Lett. 15:5213–5219. 2018.PubMed/NCBI View Article : Google Scholar | |
|
Xu L, Xu Q, Li X and Zhang X: MicroRNA-21 regulates the proliferation and apoptosis of cervical cancer cells via tumor necrosis factor-α. Mol Med Rep. 16:4659–4663. 2017.PubMed/NCBI View Article : Google Scholar | |
|
Liu F, Zhang S, Zhao Z, Mao X, Huang J, Wu Z, Zheng L and Wang Q: MicroRNA-27b up-regulated by human papillomavirus 16 E7 promotes proliferation and suppresses apoptosis by targeting polo-like kinase2 in cervical cancer. Oncotarget. 7:19666–19679. 2016.PubMed/NCBI View Article : Google Scholar | |
|
Ding H, Wu YL, Wang YX and Zhu FF: Characterization of the microRNA expression profile of cervical squamous cell carcinoma metastases. Asian Pac J Cancer Prev. 15:1675–1679. 2014.PubMed/NCBI View Article : Google Scholar | |
|
Park S, Lee S, Kim J, Kim G, Park KH, Kim TU, Chung D and Lee H: ΔNp63 to TAp63 expression ratio as a potential molecular marker for cervical cancer prognosis. PLoS One. 14(e0214867)2019.PubMed/NCBI View Article : Google Scholar | |
|
Coimbra EC, Da Conceição Gomes Leitão M, Júnior MR, De Oliveira TH, Da Costa Silva Neto J and De Freitas AC: Expression profile of microRNA-203 and its ΔNp63 target in cervical carcinogenesis: Prospects for cervical cancer screening. Anticancer Res. 36:3939–3946. 2016.PubMed/NCBI | |
|
Mandal P, Saha SS, Sen S, Bhattacharya A, Bhattacharya NP, Bucha S, Sinha M, Chowdhury RR, Mondal NR, Chakravarty B, et al: Cervical cancer subtypes harbouring integrated and/or episomal HPV16 portray distinct molecular phenotypes based on transcriptome profiling of mRNAs and miRNAs. Cell Death Discov. 5(81)2019.PubMed/NCBI View Article : Google Scholar | |
|
Balasubramaniam SD, Balakrishnan V, Oon CE and Kaur G: Key molecular events in cervical cancer development. Medicina (Kaunas). 55(384)2019.PubMed/NCBI View Article : Google Scholar | |
|
Yi Y, Liu Y, Wu W, Wu K and Zhang W: The role of miR-106p-5p in cervical cancer: From expression to molecular mechanism. Cell Death Discov. 4(36)2018.PubMed/NCBI View Article : Google Scholar | |
|
Cheng Y, Guo Y, Zhang Y, You K, Li Z and Geng L: MicroRNA-106b is involved in transforming growth factor β1-induced cell migration by targeting disabled homolog 2 in cervical carcinoma. J Exp Clin Cancer Re. 35(11)2016.PubMed/NCBI View Article : Google Scholar | |
|
Natalia MA, Alejandro GT, Virginia TJ and Alvarez-Salas LM: MARK1 is a novel target for miR-125a-5p: Implications for cell migration in cervical tumor cells. Microrna. 7:54–61. 2018.PubMed/NCBI View Article : Google Scholar | |
|
Xu Y, Zhao S, Cui M and Wang Q: Down-regulation of microRNA-135b inhibited growth of cervical cancer cells by targeting FOXO1. Int J Clin Exp Pathol. 8:10294–10304. 2015.PubMed/NCBI | |
|
Li JH, Zhang Z, Du MZ, Guan YC, Yao JN, Yu HY, Wang BJ, Wang XL, Wu SL and Li Z: MicroRNA-141-3p fosters the growth, invasion, and tumorigenesis of cervical cancer cells by targeting FOXA2. Arch Biochem Biophys. 657:23–30. 2018.PubMed/NCBI View Article : Google Scholar | |
|
Zhu J and Han S: miR-150-5p promotes the proliferation and epithelial-mesenchymal transition of cervical carcinoma cells via targeting SRCIN1. Pathol Res Pract. 215:738–747. 2019.PubMed/NCBI View Article : Google Scholar | |
|
Li N, Cui T, Guo W, Wang D and Mao L: miR-155-5p accelerates the metastasis of cervical cancer cell via targeting TP53INP1. Onco Targets Ther. 12:3181–3196. 2019.PubMed/NCBI View Article : Google Scholar | |
|
Yang M, Zhai X, Ge T, Yang C and Lou G: miR-181a-5p promotes proliferation and invasion and inhibits apoptosis of cervical cancer cells via regulating inositol polyphosphate-5-phosphatase A (INPP5A). Oncol Res. 26:703–712. 2018.PubMed/NCBI View Article : Google Scholar | |
|
Farzanehpour M, Mozhgani SH, Jalilvand S, Faghihloo E, Akhavan S, Salimi V and Azad TM: Serum and tissue miRNAs: Potential biomarkers for the diagnosis of cervical cancer. Virol J. 16(116)2019.PubMed/NCBI View Article : Google Scholar | |
|
Hou T, Ou J, Zhao X, Huang X, Huang Y and Zhang Y: MicroRNA-196a promotes cervical cancer proliferation through the regulation of FOXO1 and p27Kip1. Br J Cancer. 110:1260–1268. 2014.PubMed/NCBI View Article : Google Scholar | |
|
Varghese VK, Shukla V, Jishnu PV, Kabekkodu SP, Pandey D, Sharan K and Satyamoorthy K: Characterizing methylation regulated miRNA in carcinoma of the human uterine cervix. Life Sci. 232(116668)2019.PubMed/NCBI View Article : Google Scholar | |
|
Zhou LL, Shen Y, Gong JM, Sun P and Sheng JH: MicroRNA-466 with tumor markers for cervical cancer screening. Oncotarget. 8:70821–70827. 2017.PubMed/NCBI View Article : Google Scholar | |
|
Chu Y, Ouyang Y, Wang F, Zheng A, Bai L, Han L, Chen Y and Wang H: MicroRNA-590 promotes cervical cancer cell growth and invasion by targeting CHL1. J Cell Biochem. 115:847–853. 2014.PubMed/NCBI View Article : Google Scholar | |
|
Guerrero-Gómez AO and Guerrero-Florez M: MicroRNAs asociados al Cáncer de Cuello Uterino y sus lesiones precursoras: Una revisión sistemática. Univ Salud. 18:345–363. 2016. | |
|
Zhang H, Lu Y, Wang S, Sheng X and Zhang S: MicroRNA-152 acts as tumor suppressor microRNA by inhibiting Krüppel-like factor 5 in human cervical cancer. Oncol Res. 27:335–340. 2019.PubMed/NCBI View Article : Google Scholar | |
|
Wang S, Gao B, Yang H, Liu X, Wu X and Wang W: MicroRNA-432 is downregulated in cervical cancer and directly targets FN1 to inhibit cell proliferation and invasion. Oncol Lett. 18:1475–1482. 2019.PubMed/NCBI View Article : Google Scholar | |
|
Lu Y, Hu J, Sun W, Li S, Deng S and Li M: miR-29c inhibits cell growth, invasion, and migration of pancreatic cancer by targeting ITGB1. Onco Targets Ther. 9:99–109. 2015.PubMed/NCBI View Article : Google Scholar | |
|
Ma L and Li LL: miR-145 contributes to the progression of cervical carcinoma by directly regulating FSCN1. Cell Transplant. 28:1299–1305. 2019.PubMed/NCBI View Article : Google Scholar | |
|
Duan S, Wu A, Chen Z, Yang Y, Liu L and Shu Q: miR-204 regulates cell proliferation and invasion by targeting EphB2 in human cervical cancer. Oncol Res. 26:713–723. 2018.PubMed/NCBI View Article : Google Scholar | |
|
Shu L, Zhang Z and Cai Y: microRNA-204 inhibits cell migration and invasion in human cervical cancer by regulating transcription factor 12. Oncol Lett. 15:161–166. 2018.PubMed/NCBI View Article : Google Scholar | |
|
Li N, Guo X, Liu L, Wang L and Cheng R: Molecular mechanism of miR-204 regulates proliferation, apoptosis and autophagy of cervical cancer cells by targeting ATF2. Artif Cells Nanomed Biotechnol. 47:2529–2535. 2019.PubMed/NCBI View Article : Google Scholar | |
|
Shi C and Zhang Z: MicroRNA-320 suppresses cervical cancer cell viability, migration and invasion via directly targeting FOXM1. Oncol Lett. 14:3809–3816. 2017.PubMed/NCBI View Article : Google Scholar | |
|
Hong H, Zhu H, Zhao S, Wang K, Zhang N, Tian Y, Li Y, Wang Y, Lv X, Wei T, et al: The novel circCLK3/miR-320a/FoxM1 axis promotes cervical cancer progression. Cell Death Dis. 10(950)2019.PubMed/NCBI View Article : Google Scholar | |
|
Cao XM: Role of miR-337-3p and its target Rap1A in modulating proliferation, invasion, migration and apoptosis of cervical cancer cells. Cancer Biomark. 24:257–267. 2019.PubMed/NCBI View Article : Google Scholar | |
|
Hua FF, Liu SS, Zhu LH, Wang YH, Liang X, Ma N and Shi HR: miRNA-338-3p regulates cervical cancer cells proliferation by targeting MACC1 through MAPK signaling pathway. Eur Rev Med Pharmacol Sci. 21:5342–5352. 2017.PubMed/NCBI View Article : Google Scholar | |
|
Lu R, Yang Z, Xu G and Yu S: miR-338 modulates proliferation and autophagy by PI3K/AKT/mTOR signaling pathway in cervical cancer. Biomed Pharmacother. 105:633–644. 2018.PubMed/NCBI View Article : Google Scholar | |
|
Jayamohan S, Kannan M, Moorthy RK, Rajasekaran N, Jung HS, Shin YK and Arockiam AJ: Dysregulation of miR-375/AEG-1 axis by human papillomavirus 16/18-E6/E7 promotes cellular proliferation, migration, and invasion in cervical cancer. Front Oncol. 9(847)2019.PubMed/NCBI View Article : Google Scholar | |
|
Shang A, Zhou C, Bian G, Chen W, Lu W, Wang W and Li D: miR-381-3p restrains cervical cancer progression by downregulating FGF7. J Cell Biochem. 120:778–789. 2019.PubMed/NCBI View Article : Google Scholar | |
|
Teng P, Jiao Y, Hao M and Tang X: microRNA-383 suppresses the PI3K-AKT-MTOR signaling pathway to inhibit development of cervical cancer via down-regulating PARP2. J Cell Biochem. 119:5243–5252. 2018.PubMed/NCBI View Article : Google Scholar | |
|
Wang S, Zhang Y, Yuan S and Ji X: MicroRNA-485 targets MACC1 and inhibits cervical cancer cell proliferation and invasion. Mol Med Rep. 18:2407–2416. 2018.PubMed/NCBI View Article : Google Scholar | |
|
Lv M, Ou R, Zhang Q, Lin F, Li X, Wang K and Xu Y: MicroRNA-664 suppresses the growth of cervical cancer cells via targeting c-Kit. Drug Des Devel Ther. 13:2371–2379. 2019.PubMed/NCBI View Article : Google Scholar | |
|
Xu J, Wan X, Chen X, Fang Y, Cheng X, Xie X and Lu W: miR-2861 acts as a tumor suppressor via targeting EGFR/AKT2/CCND1 pathway in cervical cancer induced by human papillomavirus virus 16 E6. Sci Rep. 6(28968)2016.PubMed/NCBI View Article : Google Scholar | |
|
Jin Y, Zhou X, Yao X, Zhang Z, Cui M and Lin Y: MicroRNA-612 inhibits cervical cancer progression by targeting NOB1. J Cell Mol Med. 24:3149–3156. 2020.PubMed/NCBI View Article : Google Scholar | |
|
Zhang JJ, Wang DD, Du CX and Wang Y: Long noncoding RNA ANRIL promotes cervical cancer development by acting as a sponge of miR-186. Oncol Res. 26:345–352. 2018.PubMed/NCBI View Article : Google Scholar | |
|
Liu S, Song L, Yao H, Zhang L, Xu D, Gao F and Li Q: miR-375 is epigenetically downregulated by HPV-16 E6 mediated DNMT1 upregulation and modulates EMT of cervical cancer cells by suppressing lncRNA MALAT1. PLoS One. 11(e0163460)2016.PubMed/NCBI View Article : Google Scholar | |
|
Song H, Liu Y, Jin X, Liu Y, Yang Y, Li L, Wang X and Li G: Long non-coding RNA LINC01535 promotes cervical cancer progression via targeting the miR-214/EZH2 feedback loop. J Cell Mol Med. 23:6098–6111. 2019.PubMed/NCBI View Article : Google Scholar | |
|
Sun NX, Ye C, Zhao Q, Zhang Q, Xu C, Wang SB, Jin ZJ, Sun SH, Wang F and Li W: Long noncoding RNA-EBIC promotes tumor cell invasion by binding to EZH2 and repressing E-cadherin in cervical cancer. PLoS One. 9(e100340)2014.PubMed/NCBI View Article : Google Scholar | |
|
He H, Liu X, Liu Y, Zhang M, Lai Y, Hao Y, Wang Q, Shi D, Wang N, Luo XG, et al: Human papillomavirus E6/E7 and long noncoding RNA TMPOP2 mutually upregulated gene expression in cervical cancer cells. J Virol. 93:e01808–e18. 2019.PubMed/NCBI View Article : Google Scholar | |
|
Ma Z, Shuai Y, Gao X, Wen X and Ji J: Circular RNAs in the tumour microenvironment. Mol Cancer. 19(8)2020.PubMed/NCBI View Article : Google Scholar | |
|
Bach DH, Lee SK and Sood AK: Circular RNAs in Cancer. Mol Ther Nucleic Acids. 16:118–129. 2019.PubMed/NCBI View Article : Google Scholar | |
|
Zhao J, Lee EE, Kim J, Yang R, Chamseddin B, Ni C, Gusho E, Xie Y, Chiang CM, Buszczak M, et al: Transforming activity of an oncoprotein-encoding circular RNA from human papillomavirus. Nat Commun. 10(2300)2019.PubMed/NCBI View Article : Google Scholar | |
|
Ji F, Du R, Chen T, Zhang M, Zhu Y, Luo X and Ding Y: Circular RNA circSLC26A4 accelerates cervical cancer progression via miR-1287-5p/HOXA7 axis. Mol Ther Nucleic Acids. 19:413–420. 2020.PubMed/NCBI View Article : Google Scholar | |
|
Chen RX, Liu HL, Yang LL, Kang FH, Xin LP, Huang LR, Guo QF and Wang YL: Circular RNA circRNA_0000285 promotes cervical cancer development by regulating FUS. Eur Rev Med Pharmacol Sci. 23:8771–8778. 2019.PubMed/NCBI View Article : Google Scholar | |
|
Ding S, Huang X, Zhu J, Xu B, Xu L, Gu D and Zhang W: ADH7, miR-3065 and LINC01133 are associated with cervical cancer progression in different age groups. Oncol Lett. 19:2326–2338. 2020.PubMed/NCBI View Article : Google Scholar |
