
Epigenetic approaches for cervical neoplasia screening (Review)
- Authors:
- Adrian Albulescu
- Adriana Plesa
- Alina Fudulu
- Iulia Virginia Iancu
- Gabriela Anton
- Anca Botezatu
-
Affiliations: Department of Molecular Virology, Stefan S. Nicolau Institute of Virology, Bucharest 030304, Romania - Published online on: October 25, 2021 https://doi.org/10.3892/etm.2021.10916
- Article Number: 1481
-
Copyright: © Albulescu et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
![]() |
![]() |
Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A and Bray F: Global Cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 71:209–249. 2021.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 | |
Sawaya GF, Brown AD, Washington AE and Garber AM: Current approaches to cervical-cancer screening. N Engl J Med. 344:1603–1607. 2001.PubMed/NCBI View Article : Google Scholar | |
Sawaya GF, Smith-McCune K and Kuppermann M: Cervical cancer screening: More choices in 2019. JAMA. 321:2018–2019. 2019.PubMed/NCBI View Article : Google Scholar | |
Botezatu A, Iancu IV, Plesa A, Manda D, Popa O, Bostan M, Mihaila M, Albulescu A, Fudulu A, Vladoiu SV, et al: Methylation of tumour suppressor genes associated with thyroid cancer. Cancer Biomark. 25:53–65. 2019.PubMed/NCBI View Article : Google Scholar | |
Tasca L, Ostör AG and Babeş V: XII. Aurel Babeş. Int J Gynecol Pathol. 21:198–202. 2002.PubMed/NCBI View Article : Google Scholar | |
Tan SY and Tatsumura Y: George Papanicolaou (1883-1962): Discoverer of the Pap Smear. Singapore Med J. 56:586–587. 2015.PubMed/NCBI View Article : Google Scholar | |
Petry KU, Woermann B and Schneider A: Benefits and risks of cervical cancer screening. Oncol Res Treat. 37 (Suppl 3):S48–S57. 2014.PubMed/NCBI View Article : Google Scholar | |
Lazcano-Ponce E, Lorincz AT, Cruz-Valdez A, Salmeron J, Uribe P, Velasco-Mondragón E, Nevarez PH, Acosta RD and Hernandez-Avila M: Self-collection of vaginal specimens for human papillomavirus testing in cervical cancer prevention (MARCH): A community-based randomised controlled trial. Lancet. 378:1868–1873. 2011.PubMed/NCBI View Article : Google Scholar | |
Koliopoulos G, Nyaga VN, Santesso N, Bryant P, Martin-Hirsch P, Mustafa RA, Schünemann H, Paraskevaidis E and Arbyn M: Cytology vs. HPV testing for cervical cancer screening in the general population. Cochrane Database Syst Rev. 8(CD008587)2017.PubMed/NCBI View Article : Google Scholar | |
Schmitz M, Eichelkraut K, Schmidt D, Zeiser I, Hilal Z, Tettenborn Z, Hansel A and Ikenberg H: Performance of a DNA methylation marker panel using liquid-based cervical scrapes to detect cervical cancer and its precancerous stages. BMC Cancer. 18(1197)2018.PubMed/NCBI View Article : Google Scholar | |
Wentzensen N, Schiffman M, Palmer T and Arbyn M: Triage of HPV positive women in cervical cancer screening. J Clin Virol. 76 (Suppl 1):S49–S55. 2016.PubMed/NCBI View Article : Google Scholar | |
Dillner J, Rebolj M, Birembaut P, Petry KU, Szarewski A, Munk C, de Sanjose S, Naucler P, Lloveras B, Kjaer S, et al: Long term predictive values of cytology and human papillomavirus testing in cervical cancer screening: Joint European cohort study. BMJ. 337(a1754)2008.PubMed/NCBI View Article : Google Scholar | |
Saslow D, Solomon D, Lawson HW, Killackey M, Kulasingum SL, Cain J, Garcia FAR, Moriarty AT, Waxman AG, Wilbur DC, et al: American Cancer Society, American Society for Colposcopy and Cervical Pathology and American Society for Clinical Pathology screening guidelines for the prevention and early detection of cervical cancer. CA Cancer J Clin. 62:147–172. 2012.PubMed/NCBI View Article : Google Scholar | |
Bian M, Cheng J, Ma L, Cong X, Liu J, Chen Y and Chen X: Evaluation of the detection of 14 high-risk human papillomaviruses with HPV 16 and HPV 18 genotyping for cervical cancer screening. Exp Ther Med. 6:1332–1336. 2013.PubMed/NCBI View Article : Google Scholar | |
Tian Y, Wu NYY, Liou YL, Yeh CT, Cao L, Kang YN, Wang HJ, Li Y, Chu TY, Li W, et al: Utility of gene methylation analysis, cytological examination and HPV-16/18 genotyping in triage of high-risk human papilloma virus-positive women. Oncotarget. 8:62274–62285. 2017.PubMed/NCBI View Article : Google Scholar | |
Fudulu A, Albulescu A and Anton G: Human papillomaviruses' proteins with clinical utility. J Immunoassay Immunochem. 40:81–90. 2013.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 | |
Gai W and Sun K: Epigenetic biomarkers in cell-free DNA and applications in liquid biopsy. Genes (Basel). 10(32)2019.PubMed/NCBI View Article : Google Scholar | |
Dagogo-Jack I and Shaw AT: Tumour heterogeneity and resistance to cancer therapies. Nat Rev Clin Oncol. 15:81–94. 2018.PubMed/NCBI View Article : Google Scholar | |
Baylin SB and Jones PA: Epigenetic determinants of cancer. Cold Spring Harb Perspect Biol. 8(a019505)2016.PubMed/NCBI View Article : Google Scholar | |
Lleras RA, Smith RV, Adrien LR, Schlecht NF, Burk RD, Harris TM, Childs G, Prystowsky MB and Belbin TJ: Unique DNA methylation loci distinguish anatomic site and HPV status in head and neck squamous cell carcinoma. Clin Cancer Res. 19:5444–5455. 2013.PubMed/NCBI View Article : Google Scholar | |
Wentzensen N, Sherman ME, Schiffman M and Wang SS: Utility of methylation markers in cervical cancer early detection: Appraisal of the state-of-the-science. Gynecol Oncol. 112:293–299. 2009.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 | |
Plesa A, Iancu IV, Botezatu A, Huica I, Stoian M and Anton G: The involvement of epigenetic mechanisms in HPV-induced cervical cancer, Rajamanickam Rajkumar, human papillomavirus-research in a global perspective, IntechOpen, London, 191-239, 2016. https://www.intechopen.com/chapters/50425. Accessed June, 16, 2021. | |
Du J, Johnson LM, Jacobsen SE and Patel DJ: DNA methylation pathways and their crosstalk with histone methylation. Nat Rev Mol Cell Biol. 16:519–532. 2015.PubMed/NCBI View Article : Google Scholar | |
Jin B and Robertson KD: DNA methyltransferases, DNA damage repair and cancer. Adv Exp Med Biol. 754:3–29. 2013.PubMed/NCBI View Article : Google Scholar | |
Williams K, Christensen J and Helin K: DNA methylation: TET proteins-guardians of CpG islands? EMBO Rep. 13:28–35. 2011.PubMed/NCBI View Article : Google Scholar | |
Schübeler D: Function and information content of DNA methylation. Nature. 517:321–326. 2015.PubMed/NCBI View Article : Google Scholar | |
Sina AA, Carrascosa LG, Liang Z, Grewal SY, Wardiana A, Shiddiky MJA, Gardiner RA, Samaratunga H, Gandhi MK, Scott RJ, et al: Epigenetically reprogrammed methylation landscape drives the DNA self-assembly and serves as a universal cancer biomarker. Nat Commun. 9(4915)2018.PubMed/NCBI View Article : Google Scholar | |
Kanwal R, Gupta K and Gupta S: Cancer epigenetics: An introduction. Methods Mol Biol. 1238:3–25. 2015.PubMed/NCBI View Article : Google Scholar | |
Reinert T: Methylation markers for urine-based detection of bladder cancer: The next generation of urinary markers for diagnosis and surveillance of bladder cancer. Adv Urol. 2012(503271)2012.PubMed/NCBI View Article : Google Scholar | |
de Groot JS, Pan X, Meeldijk J, van der Wall E, van Diest PJ and Moelans CB: Validation of DNA promoter hypermethylation biomarkers in breast cancer-a short report. Cell Oncol (Dordr). 37:297–303. 2014.PubMed/NCBI View Article : Google Scholar | |
Yi JM: DNA Methylation change profiling of colorectal disease: Screening towards clinical use. Life (Basel). 11(412)2021.PubMed/NCBI View Article : Google Scholar | |
Etcheverry A, Aubry M, de Tayrac M, Vauleon E, Boniface R, Guenot F, Saikali S, Hamlat A, Riffaud L, Menei P, et al: DNA methylation in glioblastoma: Impact on gene expression and clinical outcome. BMC Genomics. 11(701)2010.PubMed/NCBI View Article : Google Scholar | |
LeBlanc VG and Marra MA: DNA methylation in adult diffuse gliomas. Brief Funct Genomics. 15:491–500. 2016.PubMed/NCBI View Article : Google Scholar | |
Zhang C, Li J, Huang T, Duan S, Dai D, Jiang D, Sui X, Li D, Chen Y, Ding F, et al: Meta-analysis of DNA methylation biomarkers in hepatocellular carcinoma. Oncotarget. 7:81255–81267. 2016.PubMed/NCBI View Article : Google Scholar | |
Shen N, Du J, Zhou H, Chen N, Pan Y, Hoheisel JD, Jiang Z, Xiao L, Tao Y and Mo X: A diagnostic panel of DNA methylation biomarkers for lung adenocarcinoma. Front Oncol. 9(1281)2019.PubMed/NCBI View Article : Google Scholar | |
Yang M and Park JY: DNA methylation in promoter region as biomarkers in prostate cancer. Methods Mol Biol. 863:67–109. 2012.PubMed/NCBI View Article : Google Scholar | |
Fang J, Zhang H and Jin S: Epigenetics and cervical cancer: From pathogenesis to therapy. Tumour Biol. 35:5083–5093. 2014.PubMed/NCBI View Article : Google Scholar | |
Li C, Ke J, Liu J and Su J: DNA methylation data-based molecular subtype classification related to the prognosis of patients with cervical cancer. J Cell Biochem. 121:2713–2724. 2020.PubMed/NCBI View Article : Google Scholar | |
Hernández-López R, Lorincz AT, Torres-Ibarra L, Reuter C, Scibior-Bentkowska D, Warman R, Nedjai B, Mendiola-Pastrana I, León-Maldonado L, Rivera-Paredez B, et al: Methylation estimates the risk of precancer in HPV-infected women with discrepant results between cytology and HPV16/18 genotyping. Clin Epigenetics. 11(140)2019.PubMed/NCBI View Article : Google Scholar | |
Lorincz AT: Cancer diagnostic classifiers based on quantitative DNA methylation. Expert Rev Mol Diagn. 14:293–305. 2016.PubMed/NCBI View Article : Google Scholar | |
Clarke MA, Luhn P, Gage JC, Bodelon C, Dunn ST, Walker J, Zuna R, Hewitt S, Killian JK, Yan L, et al: Discovery and validation of candidate host DNA methylation markers for detection of cervical precancer and cancer. Int J Cancer. 141:701–710. 2017.PubMed/NCBI View Article : Google Scholar | |
Kremer WW, Van Zummeren M, Novianti PW, Richter KL, Verlaat W, Snijders PJF, Heideman DAM, Steenbergen RDM, Dreyer G and Meijer CJ: Detection of hypermethylated genes as markers for cervical screening in women living with HIV. J Int AIDS Soc. 21(e25165)2018.PubMed/NCBI View Article : Google Scholar | |
Verlaat W, Van Leeuwen RW, Novianti PW, Schuuring E, Meijer CJLM, Van Der Zee AGJ, Snijders PJF, Heideman DAM, Steenbergen RDM and Wisman GBA: Host-cell DNA methylation patterns during high-risk HPV-induced carcinogenesis reveal a heterogeneous nature of cervical pre-cancer. Epigenetics. 13:769–778. 2018.PubMed/NCBI View Article : Google Scholar | |
Kong L, Wang L, Wang Z, Xiao X, Xu T, Wu H, Wu M, Liu P and Li L: DNA methylation for cervical cancer screening: A training set in China. Clin Epigenetics. 12(91)2020.PubMed/NCBI View Article : Google Scholar | |
Shivapurkar N and Gazdar AF: DNA methylation-based biomarkers in non-invasive cancer screening. Curr Mol Med. 10:123–132. 2010.PubMed/NCBI View Article : Google Scholar | |
Varghese VK, Shukla V, Kabekkodu SP, Pandey D and Satyamoorthy K: DNA methylation regulated microRNAs in human cervical cancer. Mol Carcinog. 57:370–382. 2018.PubMed/NCBI View Article : Google Scholar | |
Botezatu A, Goia-Rusanu CD, Iancu IV, Huica I, Plesa A, Socolov D, Ungureanu C and Anton G: Quantitative analysis of the relationship between microRNA-124a,-34b and-203 gene methylation and cervical oncogenesis. Mol Med Rep. 4:121–128. 2011.PubMed/NCBI View Article : Google Scholar | |
Ehrlich M: DNA hypomethylation in cancer cells. Epigenomics. 1:239–259. 2009.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 | |
Thangavelu PU, Krenács T, Dray E and Duijf PHG: In epithelial cancers, aberrant COL17A1 promoter methylation predicts its misexpression and increased invasion. Clin Epigenet. 8(120)2016.PubMed/NCBI View Article : Google Scholar | |
García AD, Abba MC, Briceño I, Aristizabal FA and Arregui AC: DNA methylation pattern in high-grade cervical intraepithelial neoplasia and cancer revealed by genomewide methylation analysis of cervical DNA. Integr Mol Med. 4:1–13. 2017.doi: 10.15761/IMM.1000309. | |
Miller JL and Grant PA: The role of DNA methylation and histone modifications in transcriptional regulation in humans. Subcell Biochem. 61:289–317. 2013.PubMed/NCBI View Article : Google Scholar | |
Greer EL and Shi Y: Histone methylation: A dynamic mark in health, disease and inheritance. Nat Rev Genet. 13:343–357. 2012.PubMed/NCBI View Article : Google Scholar | |
Bannister AJ and Kouzarides T: Regulation of chromatin by histone modifications. Cell Res. 21:381–395. 2011.PubMed/NCBI View Article : Google Scholar | |
D'Oto A, Tian QW, Davidoff AM and Yang J: Histone demethylases and their roles in cancer epigenetics. J Med Oncol Ther. 1:34–40. 2016.PubMed/NCBI | |
Groves IJ, Drane ELA, Michalski M, Monahan JM, Scarpini CG, Smith SP, Bussotti G, Várnai C, Schoenfelder S, Fraser P, et al: Three-dimensional interactions between integrated HPV genomes and cellular chromatin dysregulate host gene expression in early cervical carcinogenesis. bioRxiv: Feb. 3, 2021 2021 (Epub ahead of print). doi: 10.1101/2021.02.03.429496. | |
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 | |
Mac M and Moody CA: Epigenetic regulation of the human papillomavirus life cycle. Pathogens. 9(483)2020.PubMed/NCBI View Article : Google Scholar | |
Shadeo A, Chari R, Lonergan KM, Pusic A, Miller D, Ehlen T, Van Niekerk D, Matisic J, Richards-Kortum R, Follen M, et al: Up regulation in gene expression of chromatin remodelling factors in cervical intraepithelial neoplasia. BMC Genomics. 9(64)2008.PubMed/NCBI View Article : Google Scholar | |
Kanwal R and Gupta S: Epigenetic modifications in cancer. Clin Genet. 81:303–311. 2012.PubMed/NCBI View Article : Google Scholar | |
Lu Y, Chan YT, Tan HY, Li S, Wang N and Feng Y: Epigenetic regulation in human cancer: The potential role of epi-drug in cancer therapy. Mol Cancer. 19(79)2020.PubMed/NCBI View Article : Google Scholar | |
Feng C, Dong J, Chang W, Cui M and Xu T: The progress of methylation regulation in gene expression of cervical cancer. Int J Genomics. 2018(8260652)2018.PubMed/NCBI View Article : Google Scholar | |
Rathinasamy B and Velmurugan BK: Role of lncRNAs in the cancer development and progression and their regulation by various phytochemicals. Biomed Pharmacother. 102:242–248. 2018.PubMed/NCBI View Article : Google Scholar | |
Wang X, Wang HK, Li Y, Hafner M, Banerjee NS, Tang S, Briskin D, Meyers C, Chow LT, Xie X, et al: microRNAs are biomarkers of oncogenic human papillomavirus infections. Proc Natl Acad Sci USA. 111:4262–4267. 2014.PubMed/NCBI View Article : Google Scholar | |
Jia W, Wu Y, Zhang Q, Gao GE, Zhang C and Xiang Y: Expression profile of circulating microRNAs as a promising fingerprint for cervical cancer diagnosis and monitoring. Mol Clin Oncol. 3:851–858. 2015.PubMed/NCBI View Article : Google Scholar | |
Kong Q, Tang Z, Xiang F, Jiang J, Yue H, Wu R and Kang X: Diagnostic value of Serum hsa-mir-92a in patients with cervical cancer. Clin Lab. 63:335–340. 2017.PubMed/NCBI View Article : Google Scholar | |
Laengsri V, Kerdpin U, Plabplueng C, Treeratanapiboon L and Nuchnoi P: Cervical cancer markers: Epigenetics and microRNAs. Lab Med. 49:97–111. 2018.PubMed/NCBI View Article : Google Scholar | |
Gibb EA, Becker-Santos DD, Enfield KS, Guillaud M, Niekerk Dv, Matisic JP, Macaulay CE and Lam WL: Aberrant expression of long noncoding RNAs in cervical intraepithelial neoplasia. Int J Gynecol Cancer. 22:1557–1563. 2012.PubMed/NCBI View Article : Google Scholar | |
Aalijahan H and Ghorbian S: Long non-coding RNAs and cervical cancer. Exp Mol Pathol. 106:7–16. 2019.PubMed/NCBI View Article : Google Scholar | |
Burgers WA, Blanchon L, Pradhan S, de Launoit Y, Kouzarides T and Fuks F: Viral oncoproteins target the DNA methyltransferases. Oncogene. 26:1650–1655. 2007.PubMed/NCBI View Article : Google Scholar | |
Laurson J, Khan S, Chung R, Cross K and Raj K: Epigenetic repression of E-cadherin by human papillomavirus 16 E7 protein. Carcinogenesis. 31:918–926. 2010.PubMed/NCBI View Article : Google Scholar | |
Leonard SM, Wei W, Collins SI, Pereira M, Diyaf A, Constandinou-Williams C, Young LS, Roberts S and Woodman CB: Oncogenic human papillomavirus imposes an instructive pattern of DNA methylation changes which parallel the natural history of cervical HPV infection in young women. Carcinogenesis. 33:1286–1293. 2012.PubMed/NCBI View Article : Google Scholar | |
Hsu CH, Peng KL, Jhang HC, Lin CH, Wu SY, Chiang CM, Lee SC, Yu WC and Juan LJ: The HPV E6 oncoprotein targets histone methyltransferases for modulating specific gene transcription. Oncogene. 31:2335–2349. 2012.PubMed/NCBI View Article : Google Scholar | |
Patel D, Huang SM, Baglia LA and McCance DJ: The E6 protein of human papillomavirus type 16 binds to and inhibits co-activation by CBP and p300. EMBO J. 18:5061–5072. 1999.PubMed/NCBI View Article : Google Scholar | |
Bernat A, Avvakumov N, Mymryk JS and Banks L: Interaction between the HPV E7 oncoprotein and the transcriptional coactivator p300. Oncogene. 22:7871–7881. 2003.PubMed/NCBI View Article : Google Scholar | |
Thomas MC and Chiang CM: E6 oncoprotein represses p53-dependent gene activation via inhibition of protein acetylation independently of inducing p53 degradation. Mol Cell. 17:251–264. 2005.PubMed/NCBI View Article : Google Scholar | |
Avvakumov N, Torchia J and Mymryk JS: Interaction of the HPV E7 proteins with the pCAF acetyltransferase. Oncogene. 22:3833–3841. 2003.PubMed/NCBI View Article : Google Scholar | |
Huang SM and McCance DJ: Down regulation of the interleukin-8 promoter by human papillomavirus type 16 E6 and E7 through effects on CREB binding protein/p300 and P/CAF. J Virol. 76:8710–8721. 2002.PubMed/NCBI View Article : Google Scholar | |
Münger K, Baldwin A, Edwards KM, Hayakawa H, Nguyen CL, Owens M, Grace M and Huh K: Mechanisms of human papillomavirus-induced oncogenesis. J Virol. 78:11451–11460. 2004.PubMed/NCBI View Article : Google Scholar | |
Jha S, Vande Pol S, Banerjee NS, Dutta AB, Chow LT and Dutta A: Destabilization of TIP60 by human papillomavirus E6 results in attenuation of TIP60-dependent transcriptional regulation and apoptotic pathway. Mol Cell. 38:700–711. 2010.PubMed/NCBI View Article : Google Scholar | |
Brehm A, Nielsen SJ, Miska EA, McCance DJ, Reid JL, Bannister AJ and Kouzarides T: The E7 oncoprotein associates with Mi2 and histone deacetylase activity to promote cell growth. EMBO J. 18:2449–2458. 1999.PubMed/NCBI View Article : Google Scholar | |
Longworth MS and Laimins LA: The binding of histone deacetylases and the integrity of zinc finger-like motifs of the E7 protein are essential for the life cycle of human papillomavirus type 31. J Virol. 78:3533–3541. 2004.PubMed/NCBI View Article : Google Scholar | |
Longworth MS, Wilson R and Laimins LA: HPV31 E7 facilitates replication by activating E2F2 transcription through its interaction with HDACs. EMBO J. 24:1821–1830. 2005.PubMed/NCBI View Article : Google Scholar | |
McLaughlin-Drubin ME, Crum CP and Münger K: Human papillomavirus E7 oncoprotein induces KDM6A and KDM6B histone demethylase expression and causes epigenetic reprogramming. Proc Natl Acad Sci USA. 108:2130–2135. 2011.PubMed/NCBI View Article : Google Scholar | |
Wang Y, Tong J, Lin H, Ma L and Xu Y: CCHE1 accelerated the initiation of oral squamous cell carcinoma through enhancing PAK2 expression by sponging miR-922. J Oral Pathol Med. 49:636–644. 2020.PubMed/NCBI View Article : Google Scholar | |
Sharma S, Mandal P, Sadhukhan T, Roy Chowdhury R, Ranjan Mondal N, Chakravarty B, Chatterjee T, Roy S and Sengupta S: Bridging links between long noncoding RNA HOTAIR and HPV oncoprotein E7 in cervical cancer pathogenesis. Sci Rep. 5(11724)2015.PubMed/NCBI View Article : Google Scholar | |
Zhang J and Gao Y: Long non-coding RNA MEG3 inhibits cervical cancer cell growth by promoting degradation of P-STAT3 protein via ubiquitination. Cancer Cell Int. 19(175)2019.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:e01808–18. 2019.PubMed/NCBI View Article : Google Scholar | |
Wang X, Wang HK, McCoy JP, Banerjee NS, Rader JS, Broker TR, Meyers C, Chow LT and Zheng ZM: Oncogenic HPV infection interrupts the expression of tumor-suppressive miR-34a through viral oncoprotein E6. RNA. 15:637–647. 2009.PubMed/NCBI View Article : Google Scholar | |
Melar-New M and Laimins LA: Human papillomaviruses modulate expression of microRNA 203 upon epithelial differentiation to control levels of p63 proteins. J Virol. 84:5212–5221. 2010.PubMed/NCBI View Article : Google Scholar | |
Yao T and Lin Z: MiR-21 is involved in cervical squamous cell tumorigenesis and regulates CCL20. Biochim Biophys Acta. 1822:248–260. 2012.PubMed/NCBI View Article : Google Scholar | |
Kottaridi C, Leventakou D, Pouliakis A, Pergialiotis V, Chrelias G, Patsouri E, Zacharatou A, Panopoulou E, Damaskou V, Sioulas V, et al: Searching HPV genome for methylation sites involved in molecular progression to cervical precancer. J Cancer. 10:4588–4595. 2019.PubMed/NCBI View Article : Google Scholar | |
Hsu YW, Huang RL, Su PH, Chen YC, Wang HC, Liao CC and Lai HC: Genotype-specific methylation of HPV in cervical intraepithelial neoplasia. J Gynecol Oncol. 28(e56)2017.PubMed/NCBI View Article : Google Scholar | |
Lorincz AT, Brentnall AR, Scibior-Bentkowska D, Reuter C, Banwait R, Cadman L, Austin J, Cuzick J and Vasiljević N: Validation of a DNA methylation HPV triage classifier in a screening sample. Int J Cancer. 138:2745–2751. 2016.PubMed/NCBI View Article : Google Scholar | |
Gu YY, Zhou GN, Wang Q, Ding JX and Hua KQ: Evaluation of a methylation classifier for predicting pre-cancer lesion among women with abnormal results between HPV16/18 and cytology. Clin Epigenetics. 12(57)2020.PubMed/NCBI View Article : Google Scholar | |
Sahasrabuddhe VV, Luhn P and Wentzensen N: Human papillomavirus and cervical cancer: Biomarkers for improved prevention efforts. Future Microbiol. 6:1083–1098. 2011.PubMed/NCBI View Article : Google Scholar | |
Wilting SM and Steenbergen RDM: Molecular events leading to HPV-induced high grade neoplasia. Papillomavirus Res. 2:85–88. 2016.PubMed/NCBI View Article : Google Scholar | |
Au Yeung CL, Tsang WP, Tsang TY, Co NN, Yau PL and Kwok TT: HPV-16 E6 upregulation of DNMT1 through repression of tumor suppressor p53. Oncol Rep. 24:1599–1604. 2010.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 | |
Leonard SM, Wei W, Collins SI, Pereira M, Diyaf A, Constandinou-Williams C, Young LS, Roberts S and Woodman CB: Oncogenic human papillomavirus imposes an instructive pattern of DNA methylation changes which parallel the natural history of cervical HPV infection in young women. Carcinogenesis. 33:1286–1293. 2012.PubMed/NCBI View Article : Google Scholar | |
Kalantari M, Osann K, Calleja-Macias IE, Kim S, Yan B, Jordan S, Chase DM, Tewari KS and Bernard HU: Methylation of human papillomavirus 16, 18, 31, and 45 L2 and L1 genes and the cellular DAPK gene: Considerations for use as biomarkers of the progression of cervical neoplasia. Virology. 448:314–321. 2014.PubMed/NCBI View Article : Google Scholar | |
Brentnall AR, Vasiljević N, Scibior-Bentkowska D, Cadman L, Austin J, Szarewski A, Cuzick J and Lorincz AT: A DNA methylation classifier of cervical precancer based on human papillomavirus and human genes. Int J Cancer. 135:1425–1432. 2014.PubMed/NCBI View Article : Google Scholar | |
Brentnall AR, Vasiljevic N, Scibior-Bentkowska D, Cadman L, Austin J, Cuzick J and Lorincz AT: DNA methylation assay for HPV33 contributes independent triage information to HPV16, HPV18, HPV31, and EPB41L3 for detecting cervical pre-cancer. Cancer Biomark. 15:669–675. 2015.PubMed/NCBI View Article : Google Scholar | |
Qiagen: Products: Cervical Cancer Screening. https://www.qiagen.com/be/products/diagnostics-and-clinical-research/sexual-reproductive-health/cervical-cancer-screening/qiasure-methylation-test-kit-eu/#productdetails. Accessed June 16, 2021. | |
Dippmann C, Schmitz M, Wunsch K, Schütze S, Beer K, Greinke C, Ikenberg H, Hoyer H, Runnebaum IB, Hansel A and Dürst M: Triage of hrHPV-positive women: Comparison of two commercial methylation-specific PCR assays. Clin Epigenetics. 12(171)2020.PubMed/NCBI View Article : Google Scholar | |
Schmitz M, Eichelkraut K, Schmidt D, Zeiser I, Hilal Z, Tettenborn Z, Hansel A and Ikenberg H: Performance of a DNA methylation marker panel using liquid-based cervical scrapes to detect cervical cancer and its precancerous stages. BMC Cancer. 18(1197)2018.PubMed/NCBI View Article : Google Scholar | |
Kocsis A, Takács T, Jeney C, Schaff Z, Koiss R, Járay B, Sobel G, Pap K, Székely I, Ferenci T, et al: Performance of a new HPV and biomarker assay in the management of hrHPV positive women: Subanalysis of the ongoing multicenter TRACE clinical trial (n > 6,000) to evaluate POU4F3 methylation as a potential biomarker of cervical precancer and cancer. Int J Cancer. 140:1119–1133. 2017.PubMed/NCBI View Article : Google Scholar | |
Kan YY, Liou YL, Wang HJ, Chen CY, Sung LC, Chang CF and Liao CI: PAX1 methylation as a potential biomarker for cervical cancer screening. Int J Gynecol Cancer. 24:928–934. 2014.PubMed/NCBI View Article : Google Scholar | |
Liou YL, Zhang TL, Yan T, Yeh CT, Kang YN, Cao L, Wu N, Chang CF, Wang HJ, et al: Combined clinical and genetic testing algorithm for cervical cancer diagnosis. Clin Epigenetics. 8(66)2016.PubMed/NCBI View Article : Google Scholar | |
Witjes JA, Morote J, Cornel EB, Gakis G, van Valenberg FJP, Lozano F, Sternberg IA, Willemsen E, Hegemann ML, Paitan Y and Leibovitch I: Performance of the Bladder EpiCheck™ Methylation Test for Patients Under Surveillance for Non-muscle-invasive Bladder Cancer: Results of a Multicenter, Prospective, Blinded Clinical Trial. Eur Urol Oncol. 1:307–313. 2018.PubMed/NCBI View Article : Google Scholar | |
Wasserstrom A, Frumkin D, Dotan Z, Bukin E, Gadish T, Hanuka S, Knirsh R, Darawsha AE and Leibovitch I: MP13-15 molecular urine cytology-bladder epicheck is a novel molecular diagnostic tool for monitoring of bladder cancer patients. J Urol. 195(e140)2016. | |
D'Andrea D, Soria F, Zehetmayer S, Gust KM, Korn S, Witjes JA and Shariat SF: Diagnostic accuracy, clinical utility and influence on decision-making of a methylation urine biomarker test in the surveillance of non-muscle-invasive bladder cancer. BJU Int. 123:959–967. 2019.PubMed/NCBI View Article : Google Scholar | |
Su SF, de Castro Abreu AL, Chihara Y, Tsai Y, Andreu-Vieyra C, Daneshmand S, Skinner EC, Jones PA, Siegmund KD and Liang G: A panel of three markers hyper- and hypomethylated in urine sediments accurately predicts bladder cancer recurrence. Clin Cancer Res. 20:1978–1989. 2014.PubMed/NCBI View Article : Google Scholar | |
Van Kessel KE, Beukers W, Lurkin I, Ziel-van der Made A, van der Keur KA, Boormans JL, Dyrskjøt L, Márquez M, Ørntoft TF, Real FX, et al: Validation of a DNA Methylation-Mutation Urine Assay to Select Patients with Hematuria for Cystoscopy. J Urol. 197:590–595. 2017.PubMed/NCBI View Article : Google Scholar | |
Feber A, Dhami P, Dong L, de Winter P, Tan WS, Martínez-Fernández M, Paul DS, Hynes-Allen A, Rezaee S, Gurung P, et al: UroMark-a urinary biomarker assay for the detection of bladder cancer. Clin Epigenetics. 9(8)2017.PubMed/NCBI View Article : Google Scholar | |
Maier S, Nimmrich I, Koenig T, Eppenberger-Castori S, Bohlmann I, Paradiso A, Spyratos F, Thomssen C, Mueller V, Nährig J, et al: DNA-methylation of the homeodomain transcription factor PITX2 reliably predicts risk of distant disease recurrence in tamoxifen-treated, node-negative breast cancer patients-Technical and clinical validation in a multi-centre setting in collaboration with the European Organisation for Research and Treatment of Cancer (EORTC) PathoBiology group. Eur J Cancer. 43:1679–1686. 2007.PubMed/NCBI View Article : Google Scholar | |
Imperiale TF, Ransohoff DF, Itzkowitz SH, Levin TR, Lavin P, Lidgard GP, Ahlquist DA and Berger BM: Multitarget stool DNA testing for colorectal-cancer screening. N Engl J Med. 370:1287–1297. 2014.PubMed/NCBI View Article : Google Scholar | |
Oussalah A, Rischer S, Bensenane M, Conroy G, Filhine-Tresarrieu P, Debard R, Forest-Tramoy D, Josse T, Reinicke D, Garcia M, et al: Plasma mSEPT9: A novel circulating cell-free DNA-based epigenetic biomarker to diagnose hepatocellular carcinoma. EBioMedicine. 30:138–147. 2018.PubMed/NCBI View Article : Google Scholar | |
Chalasani NP, Ramasubramanian T, Bruinsma JJ, Allawi HT, Olson M, Roberts LR, Kisiel J, Reddy KR, Lidgard GP, et al: Combined methylated DNA and protein markers: An accurate blood-based test for early-stage detection of Hepatocellular carcinoma. Hepatology. 70 (Suppl 1)(109)2019. | |
Taggart D, Roy D, Li G, Liu D, Zheng L and Zhang K: DNA methylation biomarkers for noninvassive detection of hepatocellular carcinoma [abstract]. SITC 2018 Abstracts 263, 2018. https://sitc.sitcancer.org/2018/abstracts/titles/poster/. | |
Johannessen LE, Brandal P, Myklebust T, Heim S, Micci F and Panagopoulos I: MGMT Gene Promoter methylation status-Assessment of two pyrosequencing kits and three methylation-specific PCR methods for their predictive capacity in glioblastomas. Cancer Genomics Proteomics. 15:437–448. 2018.PubMed/NCBI View Article : Google Scholar | |
Gilbert MR, Dignam JJ, Armstrong TS, Wefel JS, Blumenthal DT, Vogelbaum MA, Colman H, Chakravarti A, Pugh S, Won M, et al: A randomized trial of bevacizumab for newly diagnosed glioblastoma. N Engl J Med. 370:699–708. 2014.PubMed/NCBI View Article : Google Scholar | |
Waterhouse RL Jr, Van Neste L, Moses KA, Barnswell C, Silberstein JL, Jalkut M, Tutrone R, Sylora J, Anglade R, Murdock M, et al: Evaluation of an epigenetic assay for predicting repeat prostate biopsy outcome in African American men. Urology. 128:62–65. 2019.PubMed/NCBI View Article : Google Scholar | |
Weiss G, Schlegel A, Kottwitz D, König T and Tetzner R: Validation of the SHOX2/PTGER4 DNA Methylation Marker Panel for Plasma-Based Discrimination between Patients with Malignant and Nonmalignant Lung Disease. J Thorac Oncol. 12:77–84. 2017.PubMed/NCBI View Article : Google Scholar | |
Hao YX, Fu Q, Guo YY, Ye M, Zhao HX, Wang Q, Peng XM, Li QW, Wang RL and Xiao WH: Effectiveness of circulating tumor DNA for detection of KRAS gene mutations in colorectal cancer patients: A meta-analysis. Onco Targets Ther. 10:945–953. 2017.PubMed/NCBI View Article : Google Scholar | |
Moran S, Martínez-Cardús A, Sayols S, Musulén E, Balañá C, Estival-Gonzalez A, Moutinho C, Heyn H, Diaz-Lagares A, de Moura MC, et al: Epigenetic profiling to classify cancer of unknown primary: A multicentre, retrospective analysis. Lancet Oncol. 17:1386–1395. 2016.PubMed/NCBI View Article : Google Scholar | |
Snoek BC, Splunter APV, Bleeker MCG, Ruiten MC, Heideman DAM, Rurup WF, Verlaat W, Schotman H, Gent MV, Trommel NEV and Steenbergen RDM: Cervical cancer detection by DNA methylation analysis in urine. Sci Rep. 9(3088)2019.PubMed/NCBI View Article : Google Scholar | |
Darwiche N: Epigenetic mechanisms and the hallmarks of cancer: An intimate affair. Am J Cancer Res. 10:1954–1978. 2020.PubMed/NCBI | |
Locke WJ, Guanzon D, Ma C, Liew YJ, Duesing KR, Fung KYC and Ross JP: DNA methylation cancer biomarkers: Translation to the clinic. Front Genet. 10(1150)2019.PubMed/NCBI View Article : Google Scholar | |
Keller S, Ridinger J, Rupp AK, Janssen JW and Altevogt P: Body fluid derived exosomes as a novel template for clinical diagnostics. J Transl Med. 9(86)2011.PubMed/NCBI View Article : Google Scholar | |
Meng Y, Sun J, Wang X, Hu T, Ma Y, Kong C, Piao H, Yu T and Zhang G: Exosomes: A promising avenue for the diagnosis of breast cancer. Technol Cancer Res Treat. 18(1533033818821421)2019.PubMed/NCBI View Article : Google Scholar | |
Bolha L, Ravnik-Glavač M and Glavač D: Long Noncoding RNAs as biomarkers in cancer. Dis Markers. 2017(7243968)2017.PubMed/NCBI View Article : Google Scholar |