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Published in: BMC Cancer 1/2023

Open Access 01-12-2023 | Human Papillomavirus | Research

The analysis of HPV integration sites based on nanopore sequencing and the profiling changes along the course of photodynamic therapy

Authors: Xiulan Li, Xiaoke Wei, Xin Liu, Nan Wang, Fuqiang Xu, Xingyu Liu, Yanmei Li, Yuxiang Zhou, Huadong Tang, Meina Bian, Ying Hou, Lili Zhang, Weiwei Wang, Qing Liu

Published in: BMC Cancer | Issue 1/2023

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Abstract

Objective

To detect the HPV genotype and integration sites in patients with high-risk HPV infection at different stages of photodynamic therapy using nanopore technology and to evaluate the treatment effect.

Methods

Four patients with HPV infection were selected and subjected to photodynamic therapy, and cervical exfoliated cell was sampled at before treatment, after three courses of treatment and six courses of treatment, their viral abundance and insertion sites were analyzed by nanopore technology, and pathological examinations were performed before and after treatment. In this study, we developed a novel assay that combined viral sequence enrichment and Nanopore sequencing for identification of HPV genotype and integration sites at once. The assay has obvious advantages over qPCR or NGS-based methods, as it has better sensitivity after viral sequences enrichment and can generate long-reads (kb to Mb) for better detection rate of structure variations, moreover, fast turn-around time for real-time viral sequencing and analysis.

Results

The pathological grade was reduced in all four patients after photodynamic therapy. Virus has been cleared in two cases after treatment, the virus amount reduced after treatment but not completely cleared in one case, and two type viruses were cleared and one type virus persisted after treatment in the last patient with multiple infection. Viral abundance and the number of integration sites were positively correlated. Gene enrichment analysis showed complete viral clearance in 1 patient and 3 patients required follow-up.

Conclusion

Nanopore sequencing can effectively monitor the abundance of HPV viruses and integration sites to show the presence status of viruses, and combined with the results of gene enrichment analysis, the treatment effect can be dynamically assessed.
Literature
1.
go back to reference Zur HH. Papillomavirus infections: a major cause of human cancers [M]. Biochim Biophys Acta. 1996;1288(2):55–78. Zur HH. Papillomavirus infections: a major cause of human cancers [M]. Biochim Biophys Acta. 1996;1288(2):55–78.
2.
go back to reference Chen Z, Freitas LBD, Burk RD. Evolution and classification of oncogenic human papillomavirus types and variants associated with cervical cancer [J]. Methods Mol Biol. 2015;1249:3–26.PubMedPubMedCentralCrossRef Chen Z, Freitas LBD, Burk RD. Evolution and classification of oncogenic human papillomavirus types and variants associated with cervical cancer [J]. Methods Mol Biol. 2015;1249:3–26.PubMedPubMedCentralCrossRef
3.
go back to reference Bernard HU, Burk RD, Chen Z, et al. Classification of papillomaviruses (PVs) based on 189 PV types and proposal of taxonomic amendments [J]. Virology. 2010;401(1):70–9.PubMedCrossRef Bernard HU, Burk RD, Chen Z, et al. Classification of papillomaviruses (PVs) based on 189 PV types and proposal of taxonomic amendments [J]. Virology. 2010;401(1):70–9.PubMedCrossRef
4.
go back to reference Doorbar J. Molecular biology of human papillomavirus infection and cervical cancer [J]. Clin Sci (London). 2006;110(5):525–41.CrossRef Doorbar J. Molecular biology of human papillomavirus infection and cervical cancer [J]. Clin Sci (London). 2006;110(5):525–41.CrossRef
5.
go back to reference Bernard HU, Calleja-Macias IE, Dunn ST. Genome variation of human papillomavirus types: phylogenetic and medical implications [J]. Int J Cancer. 2006;118(5):1071–6.PubMedCrossRef Bernard HU, Calleja-Macias IE, Dunn ST. Genome variation of human papillomavirus types: phylogenetic and medical implications [J]. Int J Cancer. 2006;118(5):1071–6.PubMedCrossRef
6.
go back to reference Tsakogiannis D, Gartzonika C, Levidiotou-Stefanou S, et al. Molecular approaches for HPV genotyping and HPV-DNA physical status [J]. Expert Rev Mol Med. 2017;19: e1.PubMedCrossRef Tsakogiannis D, Gartzonika C, Levidiotou-Stefanou S, et al. Molecular approaches for HPV genotyping and HPV-DNA physical status [J]. Expert Rev Mol Med. 2017;19: e1.PubMedCrossRef
7.
go back to reference Li W, Wang W, Si M, et al. The physical state of HPV16 infection and its clinical significance in cancer precursor lesion and cervical carcinoma [J]. J Cancer Res Clin Oncol. 2008;134(12):1355–61.PubMedCrossRef Li W, Wang W, Si M, et al. The physical state of HPV16 infection and its clinical significance in cancer precursor lesion and cervical carcinoma [J]. J Cancer Res Clin Oncol. 2008;134(12):1355–61.PubMedCrossRef
8.
go back to reference Hudelist G, Manavi M, Pischinger KID, et al. Physical state and expression of HPV DNA in benign and dysplastic cervical tissue: different levels of viral integration are correlated with lesion grade [J]. Gynecol Oncol. 2004;92(3):873–80.PubMedCrossRef Hudelist G, Manavi M, Pischinger KID, et al. Physical state and expression of HPV DNA in benign and dysplastic cervical tissue: different levels of viral integration are correlated with lesion grade [J]. Gynecol Oncol. 2004;92(3):873–80.PubMedCrossRef
9.
go back to reference Akagi K, Li J, Broutian TR, et al. Genome-wide analysis of HPV integration in human cancers reveals recurrent, focal genomic instability [J]. Genome Res. 2014;24(2):185–99.PubMedPubMedCentralCrossRef Akagi K, Li J, Broutian TR, et al. Genome-wide analysis of HPV integration in human cancers reveals recurrent, focal genomic instability [J]. Genome Res. 2014;24(2):185–99.PubMedPubMedCentralCrossRef
10.
go back to reference Bo X, Sasithorn C, Stephan W, et al. Multiplex identification of human papillomavirus 16 DNA integration sites in cervical carcinomas [J]. PLoS ONE. 2013;8(6): e66693.CrossRef Bo X, Sasithorn C, Stephan W, et al. Multiplex identification of human papillomavirus 16 DNA integration sites in cervical carcinomas [J]. PLoS ONE. 2013;8(6): e66693.CrossRef
12.
go back to reference Xu Y, Yuan L, Pu D, et al. The integration of human papilloma viral 16 and its relationship with FHIT expression in cervical cancer [J]. Chin J Clin Obstetr Gynecol. 2017;18(1):17–9. Xu Y, Yuan L, Pu D, et al. The integration of human papilloma viral 16 and its relationship with FHIT expression in cervical cancer [J]. Chin J Clin Obstetr Gynecol. 2017;18(1):17–9.
13.
go back to reference Zhou L, Qiu Q, Zhou Q, et al. Long-read sequencing unveils high-resolution HPV integration and its oncogenic progression in cervical cancer [J]. Nat Commun. 2022;13(1):2563–81.PubMedPubMedCentralCrossRef Zhou L, Qiu Q, Zhou Q, et al. Long-read sequencing unveils high-resolution HPV integration and its oncogenic progression in cervical cancer [J]. Nat Commun. 2022;13(1):2563–81.PubMedPubMedCentralCrossRef
14.
go back to reference Jun SY, Park ES, Kim J, et al. Comparison of the Cobas 4800 HPV and HPV 9G DNA chip tests for detection of high -risk human papillomavirus in cervical specimens of women with consecutive positive HPV tests but negative pap smears [J]. PLoS ONE. 2015;10(10):e0140336–46.PubMedPubMedCentralCrossRef Jun SY, Park ES, Kim J, et al. Comparison of the Cobas 4800 HPV and HPV 9G DNA chip tests for detection of high -risk human papillomavirus in cervical specimens of women with consecutive positive HPV tests but negative pap smears [J]. PLoS ONE. 2015;10(10):e0140336–46.PubMedPubMedCentralCrossRef
15.
go back to reference Qiu LH, Li JR, Chen F, et al. Chinese Expert Consensus on the Clinical Applications of Aminolevulinic Acid-Based Photodynamic Therapy in Female Lower Genital Tract Diseases (2022) [J]. Photodiagn Photodyn Ther. 2022;39:102993–8.CrossRef Qiu LH, Li JR, Chen F, et al. Chinese Expert Consensus on the Clinical Applications of Aminolevulinic Acid-Based Photodynamic Therapy in Female Lower Genital Tract Diseases (2022) [J]. Photodiagn Photodyn Ther. 2022;39:102993–8.CrossRef
16.
go back to reference Ran R, Wang M, Li XL, et al. A prospective study of photodynamic therapy for cervical squamous intraepithelial lesion [J]. Photodiagn Photodyn Ther. 2021;34:102185–92.CrossRef Ran R, Wang M, Li XL, et al. A prospective study of photodynamic therapy for cervical squamous intraepithelial lesion [J]. Photodiagn Photodyn Ther. 2021;34:102185–92.CrossRef
17.
go back to reference Yang WJ, Liu Y, Dong RY, et al. Accurate detection of HPV integration sites in cervical cancer samples using the nanopore MinION sequencer without error correction [J]. Front Genet. 2020;11:660–74.PubMedPubMedCentralCrossRef Yang WJ, Liu Y, Dong RY, et al. Accurate detection of HPV integration sites in cervical cancer samples using the nanopore MinION sequencer without error correction [J]. Front Genet. 2020;11:660–74.PubMedPubMedCentralCrossRef
18.
go back to reference Subramanian A, Tamayo P, Mootha VK, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles [J]. Proc Natl Acad Sci U S A. 2005;102(43):15545–50.PubMedPubMedCentralCrossRef Subramanian A, Tamayo P, Mootha VK, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles [J]. Proc Natl Acad Sci U S A. 2005;102(43):15545–50.PubMedPubMedCentralCrossRef
19.
go back to reference Mootha V, Lindgren C, Eriksson KF, et al. PGC-1α-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes [J]. Nat Genet. 2003;34:267–73.PubMedCrossRef Mootha V, Lindgren C, Eriksson KF, et al. PGC-1α-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes [J]. Nat Genet. 2003;34:267–73.PubMedCrossRef
20.
go back to reference Van Doorslaer K, Zhiwen L, et al. The Papillomavirus Episteme: a major update to the papillomavirus sequence database [J]. Nucleic Acids Res. 2016;45(D1):D499–506.PubMedPubMedCentralCrossRef Van Doorslaer K, Zhiwen L, et al. The Papillomavirus Episteme: a major update to the papillomavirus sequence database [J]. Nucleic Acids Res. 2016;45(D1):D499–506.PubMedPubMedCentralCrossRef
21.
go back to reference Bletsa G, Zagouri F, Amoutzias GD, et al. Genetic variability of the HPV16 early genes and LCR. Present and future perspectives [J]. Expert Rev Mol Med. 2021;23:e19.PubMedCrossRef Bletsa G, Zagouri F, Amoutzias GD, et al. Genetic variability of the HPV16 early genes and LCR. Present and future perspectives [J]. Expert Rev Mol Med. 2021;23:e19.PubMedCrossRef
22.
go back to reference Togtema M, Jackson R, et al. The human papillomavirus 16 European-T350G E6 variant can immortalize but not transform keratinocytes in the absence of E7 [J]. Virology. 2015;485:274–82.PubMedCrossRef Togtema M, Jackson R, et al. The human papillomavirus 16 European-T350G E6 variant can immortalize but not transform keratinocytes in the absence of E7 [J]. Virology. 2015;485:274–82.PubMedCrossRef
23.
go back to reference Graham DA, Herrington CS. HPV-16 E2 gene disruption and sequence variation in CIN 3 lesions and invasive squamous cell carcinomas of the cervix: relation to numerical chromosome abnormalities [J]. Clin Mol Pathol. 2000;53(4):201–6.CrossRef Graham DA, Herrington CS. HPV-16 E2 gene disruption and sequence variation in CIN 3 lesions and invasive squamous cell carcinomas of the cervix: relation to numerical chromosome abnormalities [J]. Clin Mol Pathol. 2000;53(4):201–6.CrossRef
24.
go back to reference Tsakogiannis D, Kyriakopoulou Z, Amoutzias G, et al. Identification of novel E6–E7 sequence variants of human papillomavirus 16 [J]. Adv Virol. 2013;158(4):821–8. Tsakogiannis D, Kyriakopoulou Z, Amoutzias G, et al. Identification of novel E6–E7 sequence variants of human papillomavirus 16 [J]. Adv Virol. 2013;158(4):821–8.
25.
go back to reference Zhe XY, Xin HZ, Pan ZZ, et al. Genetic variations in E6, E7 and the long control region of human papillomavirus type 16 among patients with cervical lesions in Xinjiang, China [J]. Cancer Cell Int. 2019;19:65.PubMedPubMedCentralCrossRef Zhe XY, Xin HZ, Pan ZZ, et al. Genetic variations in E6, E7 and the long control region of human papillomavirus type 16 among patients with cervical lesions in Xinjiang, China [J]. Cancer Cell Int. 2019;19:65.PubMedPubMedCentralCrossRef
26.
go back to reference Zhou Z, Yang H, Yang L, et al. Human papillomavirus type 16 E6 and E7 gene variations associated with cervical cancer in a Han Chinese population [J]. Infect Genet Evol. 2019;73:13–20.PubMedCrossRef Zhou Z, Yang H, Yang L, et al. Human papillomavirus type 16 E6 and E7 gene variations associated with cervical cancer in a Han Chinese population [J]. Infect Genet Evol. 2019;73:13–20.PubMedCrossRef
27.
go back to reference Niccoli S, Abraham S, Richard C, et al. The Asian-American E6 variant protein of human papillomavirus 16 alone is sufficient to promote immortalization, transformation, and migration of primary human foreskin keratinocytes [J]. J Virol. 2012;86(22):12384–96.PubMedPubMedCentralCrossRef Niccoli S, Abraham S, Richard C, et al. The Asian-American E6 variant protein of human papillomavirus 16 alone is sufficient to promote immortalization, transformation, and migration of primary human foreskin keratinocytes [J]. J Virol. 2012;86(22):12384–96.PubMedPubMedCentralCrossRef
28.
go back to reference Cuninghame S, Lees SJ, et al. Two common variants of human papillomavirus type 16 E6 differentially deregulate sugar metabolism and hypoxia signalling in permissive human keratinocytes [J]. J Gen Virol. 2017;98(9):2310–9.PubMedCrossRef Cuninghame S, Lees SJ, et al. Two common variants of human papillomavirus type 16 E6 differentially deregulate sugar metabolism and hypoxia signalling in permissive human keratinocytes [J]. J Gen Virol. 2017;98(9):2310–9.PubMedCrossRef
29.
go back to reference Plesa A, Anton G, Iancu IV, et al. Molecular variants of human papilloma virus 16 E2, E4, E5, E6 and E7 genes associated with cervical neoplasia in Romanian patients [J]. Adv Virol. 2014;159(12):3305–20. Plesa A, Anton G, Iancu IV, et al. Molecular variants of human papilloma virus 16 E2, E4, E5, E6 and E7 genes associated with cervical neoplasia in Romanian patients [J]. Adv Virol. 2014;159(12):3305–20.
30.
go back to reference Eriksson A, Herron JR, Yamada T, et al. Human papillomavirus type 16 variant lineages characterized by nucleotide sequence analysis of the E5 coding segment and the E2 hinge region [J]. J Gen Virol. 1999;80(Pt 3):595–600.PubMedCrossRef Eriksson A, Herron JR, Yamada T, et al. Human papillomavirus type 16 variant lineages characterized by nucleotide sequence analysis of the E5 coding segment and the E2 hinge region [J]. J Gen Virol. 1999;80(Pt 3):595–600.PubMedCrossRef
31.
go back to reference Tsakogiannis D, Ruether IGA, Kyriakopoulou Z, et al. Molecular and phylogenetic analysis of the HPV 16 E4 gene in cervical lesions from women in Greece [J]. Adv Virol. 2012;157(9):1729–39. Tsakogiannis D, Ruether IGA, Kyriakopoulou Z, et al. Molecular and phylogenetic analysis of the HPV 16 E4 gene in cervical lesions from women in Greece [J]. Adv Virol. 2012;157(9):1729–39.
32.
go back to reference Tsakogiannis D, Gortsilas P, Kyriakopoulou Z, et al. Sites of disruption within E1 and E2 genes of HPV16 and association with cervical dysplasia [J]. J Med Virol. 2015;87(11):1973–80.PubMedCrossRef Tsakogiannis D, Gortsilas P, Kyriakopoulou Z, et al. Sites of disruption within E1 and E2 genes of HPV16 and association with cervical dysplasia [J]. J Med Virol. 2015;87(11):1973–80.PubMedCrossRef
33.
go back to reference Hu Z, Zhu D, Wang W, et al. Genome-wide profiling of HPV integration in cervical cancer identifies clustered genomic hot spots and a potential microhomology-mediated integration mechanism [J]. Nat Genet. 2015;47(2):158–63.PubMedCrossRef Hu Z, Zhu D, Wang W, et al. Genome-wide profiling of HPV integration in cervical cancer identifies clustered genomic hot spots and a potential microhomology-mediated integration mechanism [J]. Nat Genet. 2015;47(2):158–63.PubMedCrossRef
34.
go back to reference Cricca M, Venturoli S, Leo E, et al. Disruption of HPV 16 E1 and E2 genes in precancerous cervical lesions [J]. J Virol Methods. 2009;158(1–2):180–3.PubMedCrossRef Cricca M, Venturoli S, Leo E, et al. Disruption of HPV 16 E1 and E2 genes in precancerous cervical lesions [J]. J Virol Methods. 2009;158(1–2):180–3.PubMedCrossRef
35.
go back to reference Li H, Yang Y, Zhang R, et al. Preferential sites for the integration and disruption of human papillomavirus 16 in cervical lesions [J]. J Clin Virol. 2013;56(4):342–7.PubMedCrossRef Li H, Yang Y, Zhang R, et al. Preferential sites for the integration and disruption of human papillomavirus 16 in cervical lesions [J]. J Clin Virol. 2013;56(4):342–7.PubMedCrossRef
36.
go back to reference Wang L, Dai SZ, Chu HJ, et al. Integration sites and genotype distributions of human papillomavirus in cervical intraepithelial neoplasia [J]. Asian Pac J Cancer Prev. 2013;14(6):3837–41.PubMedCrossRef Wang L, Dai SZ, Chu HJ, et al. Integration sites and genotype distributions of human papillomavirus in cervical intraepithelial neoplasia [J]. Asian Pac J Cancer Prev. 2013;14(6):3837–41.PubMedCrossRef
37.
go back to reference Arias-Pulido H, Peyton CL, Joste NE, et al. Human papillomavirus type 16 integration in cervical carcinoma in situ and in invasive cervical cancer [J]. J Clin Microbiol. 2006;44(5):1755–62.PubMedPubMedCentralCrossRef Arias-Pulido H, Peyton CL, Joste NE, et al. Human papillomavirus type 16 integration in cervical carcinoma in situ and in invasive cervical cancer [J]. J Clin Microbiol. 2006;44(5):1755–62.PubMedPubMedCentralCrossRef
38.
go back to reference Kalantari M, Karlsen F, Kristensen G, et al. Disruption of the E1 and E2 reading frames of HPV 16 in cervical carcinoma is associated with poor prognosis [J]. Int J Gynecol Pathol. 1998;17(2):146–53.PubMedCrossRef Kalantari M, Karlsen F, Kristensen G, et al. Disruption of the E1 and E2 reading frames of HPV 16 in cervical carcinoma is associated with poor prognosis [J]. Int J Gynecol Pathol. 1998;17(2):146–53.PubMedCrossRef
39.
go back to reference Chen M, Li L, Zheng PS. SALL4 promotes the tumorigenicity of cervical cancer cells through activation of the Wnt/β-catenin pathway via CTNNB1 [J]. Cancer Sci. 2019;110(9):2794–805.PubMedPubMedCentralCrossRef Chen M, Li L, Zheng PS. SALL4 promotes the tumorigenicity of cervical cancer cells through activation of the Wnt/β-catenin pathway via CTNNB1 [J]. Cancer Sci. 2019;110(9):2794–805.PubMedPubMedCentralCrossRef
40.
go back to reference Dai Y, Tong R, Guo H, et al. Association of CXCR4, CCR7, VEGF-C and VEGF-D expression with lymph node metastasis in patients with cervical cancer [J]. Eur J Obstet Gynecol Reprod Biol. 2017;214:178–83.PubMedCrossRef Dai Y, Tong R, Guo H, et al. Association of CXCR4, CCR7, VEGF-C and VEGF-D expression with lymph node metastasis in patients with cervical cancer [J]. Eur J Obstet Gynecol Reprod Biol. 2017;214:178–83.PubMedCrossRef
41.
go back to reference Chen Q, Li L, Liu X, et al. Hexokinases 2 promoted cell motility and distant metastasis by elevating fibronectin through Akt1/p-Akt1 in cervical cancer cells [J]. Cancer Cell Int. 2021;21(1):600–12.PubMedPubMedCentralCrossRef Chen Q, Li L, Liu X, et al. Hexokinases 2 promoted cell motility and distant metastasis by elevating fibronectin through Akt1/p-Akt1 in cervical cancer cells [J]. Cancer Cell Int. 2021;21(1):600–12.PubMedPubMedCentralCrossRef
42.
go back to reference Nie J, Shao J, Guo SW, et al. The relevance of plasma R-spondin 1 and Slit2 as predictive biomarkers in cervical cancer chemotherapy and radiotherapy [J]. Ann Transl Med. 2021;9(10):837–46.PubMedPubMedCentralCrossRef Nie J, Shao J, Guo SW, et al. The relevance of plasma R-spondin 1 and Slit2 as predictive biomarkers in cervical cancer chemotherapy and radiotherapy [J]. Ann Transl Med. 2021;9(10):837–46.PubMedPubMedCentralCrossRef
43.
go back to reference Ye X, Jing L, Zhong X, et al. Interactions between polymorphisms in the 3’untranslated region of the cyclin dependent kinase 6 gene and the human papillomavirus infection, and risk of cervical precancerous lesions [J]. Biomed Rep. 2017;6(6):640–8.PubMedPubMedCentralCrossRef Ye X, Jing L, Zhong X, et al. Interactions between polymorphisms in the 3’untranslated region of the cyclin dependent kinase 6 gene and the human papillomavirus infection, and risk of cervical precancerous lesions [J]. Biomed Rep. 2017;6(6):640–8.PubMedPubMedCentralCrossRef
44.
go back to reference Oh YK, Lee HJ, Jeong MH, et al. Role of activating transcription factor 3 on TAp73 stability and apoptosis in paclitaxel-treated cervical cancer cells [J]. Mol Cancer Res. 2008;6(7):1232–49.PubMedPubMedCentralCrossRef Oh YK, Lee HJ, Jeong MH, et al. Role of activating transcription factor 3 on TAp73 stability and apoptosis in paclitaxel-treated cervical cancer cells [J]. Mol Cancer Res. 2008;6(7):1232–49.PubMedPubMedCentralCrossRef
45.
go back to reference Zhang X, Zheng Z, Yingji S, et al. Downregulation of glutathione peroxidase 3 is associated with lymph node metastasis and prognosis in cervical cancer [J]. Oncol Rep. 2014;31(6):2587–92.PubMedCrossRef Zhang X, Zheng Z, Yingji S, et al. Downregulation of glutathione peroxidase 3 is associated with lymph node metastasis and prognosis in cervical cancer [J]. Oncol Rep. 2014;31(6):2587–92.PubMedCrossRef
46.
go back to reference Min Z, Pu X, Gu Z. Correlative analysis of the expression of IL-10 and Ki-67 in human cervical cancer and cervical intraepithelial neoplasias and human papillomavirus infection [J]. Oncol Lett. 2018;16(6):7189–94.PubMedPubMedCentral Min Z, Pu X, Gu Z. Correlative analysis of the expression of IL-10 and Ki-67 in human cervical cancer and cervical intraepithelial neoplasias and human papillomavirus infection [J]. Oncol Lett. 2018;16(6):7189–94.PubMedPubMedCentral
47.
go back to reference Domenici L, Tonacci A, Aretini P, et al. Inflammatory biomarkers as promising predictors of prognosis in cervical cancer patients [J]. Oncology. 2021;99(9):571–9.PubMedCrossRef Domenici L, Tonacci A, Aretini P, et al. Inflammatory biomarkers as promising predictors of prognosis in cervical cancer patients [J]. Oncology. 2021;99(9):571–9.PubMedCrossRef
48.
go back to reference Ni M, Li J, Zhao H, et al. BRD4 inhibition sensitizes cervical cancer to radiotherapy by attenuating DNA repair [J]. Oncogene. 2021;40(15):2711–24.PubMedCrossRef Ni M, Li J, Zhao H, et al. BRD4 inhibition sensitizes cervical cancer to radiotherapy by attenuating DNA repair [J]. Oncogene. 2021;40(15):2711–24.PubMedCrossRef
49.
go back to reference Chen GD, Qian DY, Li ZG, et al. Down-regulation of p16 and MGMT promotes the anti-proliferative and pro-apoptotic effects of 5-Aza-dC and radiation on cervical cancer cells [J]. Cell Biochem Funct. 2017;35(8):488–96.PubMedCrossRef Chen GD, Qian DY, Li ZG, et al. Down-regulation of p16 and MGMT promotes the anti-proliferative and pro-apoptotic effects of 5-Aza-dC and radiation on cervical cancer cells [J]. Cell Biochem Funct. 2017;35(8):488–96.PubMedCrossRef
50.
go back to reference Qu J, Lu W, Li B, et al. WWOX induces apoptosis and inhibits proliferation in cervical cancer and cell lines [J]. Int J Mol Med. 2013;31(5):1139–47.PubMedCrossRef Qu J, Lu W, Li B, et al. WWOX induces apoptosis and inhibits proliferation in cervical cancer and cell lines [J]. Int J Mol Med. 2013;31(5):1139–47.PubMedCrossRef
Metadata
Title
The analysis of HPV integration sites based on nanopore sequencing and the profiling changes along the course of photodynamic therapy
Authors
Xiulan Li
Xiaoke Wei
Xin Liu
Nan Wang
Fuqiang Xu
Xingyu Liu
Yanmei Li
Yuxiang Zhou
Huadong Tang
Meina Bian
Ying Hou
Lili Zhang
Weiwei Wang
Qing Liu
Publication date
01-12-2023
Publisher
BioMed Central
Published in
BMC Cancer / Issue 1/2023
Electronic ISSN: 1471-2407
DOI
https://doi.org/10.1186/s12885-023-11538-2

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