Review Article

HPV-mediated Cervical Cancer: A Systematic Review on Immunological Basis, Molecular Biology, and Immune Evasion Mechanisms

Author(s): Ramar Vanajothi, Natarajan Srikanth, Rajendran Vijayakumar, Manikandan Palanisamy, Sundaresan Bhavaniramya and Kumpati Premkumar*

Volume 23, Issue 8, 2022

Published on: 26 January, 2022

Page: [782 - 801] Pages: 20

DOI: 10.2174/1389450123666211221160632

Price: $65

Abstract

Background: Human papillomavirus (HPV), one of the most frequently transmitted viruses, causes several malignancies, including cervical cancer.

Aim: Owing to its unique pathogenicity, the HPV virus can persist in the host organism for a longer duration than other viruses to complete its lifecycle. During its association with the host, HPV causes various pathological conditions affecting the immune system by evading the host's immune mechanisms, thereby leading to the progression of various diseases, including cancer.

Method: To date, ~ 150 serotypes have been identified, and certain high-risk HPV types are known to be associated with genital warts and cervical cancer. As of now, two prophylactic vaccines are in use for the treatment of HPV infection; however, no effective antiviral drug is available for HPVassociated disease/infections. Numerous clinical and laboratory studies have been conducted to formulate an effective and specific vaccine against HPV infections and associated diseases.

Result: As the immunological basis of HPV infection and associated disease progress persist indistinctly, deeper insights into immune evasion mechanism and molecular biology of disease would aid in developing an effective vaccine.

Conclusion: Thus, this systematic review focuses on the immunological aspects of HPV-associated cervical cancer by uncovering immune evasion strategies adapted by HPV.

Keywords: HPV, innate immunity, cervical cancer, immune evasion, vaccines, host-pathogen interaction.

Graphical Abstract
[1]
de Villiers EM, Fauquet C, Broker TR, Bernard HU, Hausen ZH. Classification of papillomaviruses. Virology 2004; 324(1): 17-27.
[http://dx.doi.org/10.1016/j.virol.2004.03.033] [PMID: 15183049]
[2]
Doorbar J, Egawa N, Griffin H, Kranjec C, Murakami I. Human papillomavirus molecular biology and disease association. Rev Med Virol 2015; 25(1): 2-23.
[http://dx.doi.org/10.1002/rmv.1822] [PMID: 25752814]
[3]
Woodman CB, Collins SI, Young LS. The natural history of cervical HPV infection: unresolved issues. Nat Rev Cancer 2007; 7(1): 11-22.
[http://dx.doi.org/10.1038/nrc2050] [PMID: 17186016]
[4]
Gillison ML. Human papillomavirus-associated head and neck cancer is a distinct epidemiologic, clinical, and molecular entity. Semin Oncol 2004; 31(6): 744-54.
[http://dx.doi.org/10.1053/j.seminoncol.2004.09.011] [PMID: 15599852]
[5]
Syrjänen S. Human papillomavirus (HPV) in head and neck cancer. J Clin Virol 2005; 32(1): S59-66.
[http://dx.doi.org/10.1016/j.jcv.2004.11.017] [PMID: 15753013]
[6]
Bosch FX, Lorincz A, Muñoz N, Meijer CJ, Shah KV. The causal relation between human papillomavirus and cervical cancer. J Clin Pathol 2002; 55(4): 244-65.
[http://dx.doi.org/10.1136/jcp.55.4.244] [PMID: 11919208]
[7]
Parkin DM, Bray F. Chapter 2: The burden of HPV-related cancers. Vaccine 2006; 24(3): 11-25.
[http://dx.doi.org/10.1016/j.vaccine.2006.05.111] [PMID: 16949997]
[8]
Malpica A, Matisic JP, Niekirk DV, et al. Kappa statistics to measure interrater and intrarater agreement for 1790 cervical biopsy specimens among twelve pathologists: qualitative histopathologic analysis and methodologic issues. Gynecol Oncol 2005; 99(3)(1): S38-52.
[http://dx.doi.org/10.1016/j.ygyno.2005.07.040] [PMID: 16183106]
[9]
Moscicki AB. Human papillomavirus infection in adolescents. Pediatr Clin North Am 1999; 46(4): 783-807.
[http://dx.doi.org/10.1016/S0031-3955(05)70152-8] [PMID: 10494257]
[10]
Reichman RC. Human papillomaviruses. Harrison’s Principle of Internal Medicine. (15th ed.). New York: McGraw Hill 2001.
[11]
Burk RD, Kelly P, Feldman J, et al. Declining prevalence of cervicovaginal human papillomavirus infection with age is independent of other risk factors. Sex Transm Dis 1996; 23(4): 333-41.
[http://dx.doi.org/10.1097/00007435-199607000-00013] [PMID: 8836027]
[12]
World health Organization (WHO). International Agency for Research on Cancer 2018. Available from: https://gco.iarc.fr/today/data/factsheets/populations/356-india-fact-sheets.pdf
[13]
Parkin DM, Bray F, Ferlay J, Pisani P. Global cancer statistics, 2002. CA Cancer J Clin 2005; 55(2): 74-108.
[http://dx.doi.org/10.3322/canjclin.55.2.74] [PMID: 15761078]
[14]
Jemal A, Siegel R, Ward E, et al. Cancer statistics, 2008. CA Cancer J Clin 2008; 58(2): 71-96.
[http://dx.doi.org/10.3322/CA.2007.0010] [PMID: 18287387]
[15]
Braaten KP, Laufer MR. Human Papillomavirus (HPV), HPV related disease, and the HPV vaccine. Rev Obstet Gynecol 2008; 1(1): 2-10.
[PMID: 18701931]
[16]
Batson A, Meheus F, Brooke S. Innovative financing mechanisms to accelerate the introduction of HPV vaccines in developing countries. Vaccine 2006; 24(3): 219-25.
[http://dx.doi.org/10.1016/j.vaccine.2006.05.042] [PMID: 16950010]
[17]
Beutner KR, Tyring SK, Trofatter KF Jr, et al. Imiquimod, a patient-applied immune-response modifier for treatment of external genital warts. Antimicrob Agents Chemother 1998; 42(4): 789-94.
[http://dx.doi.org/10.1128/AAC.42.4.789] [PMID: 9559784]
[18]
Scheinfeld N, Lehman DS. An evidence-based review of medical and surgical treatments of genital warts. Dermatol Online J 2006; 12(3): 5.
[PMID: 16638419]
[19]
Siddiqui MA, Perry CM. Human papillomavirus quadrivalent (types 6, 11, 16, 18) recombinant vaccine (Gardasil). Drugs 2006; 66(9): 1263-71.
[http://dx.doi.org/10.2165/00003495-200666090-00008] [PMID: 16827602]
[20]
Harper DM, Franco EL, Wheeler CM, et al. Sustained efficacy up to 4.5 years of a bivalent L1 virus-like particle vaccine against human papillomavirus types 16 and 18: Follow-up from a randomised control trial. Lancet 2006; 367(9518): 1247-55.
[http://dx.doi.org/10.1016/S0140-6736(06)68439-0] [PMID: 16631880]
[21]
Giuliano AR, Palefsky JM, Goldstone S, et al. Efficacy of quadrivalent HPV vaccine against HPV Infection and disease in males. N Engl J Med 2011; 364(5): 401-11.
[http://dx.doi.org/10.1056/NEJMoa0909537] [PMID: 21288094]
[22]
Harden ME, Munger K. Human papillomavirus molecular biology. Mutat Res Rev Mutat Res 2017; 772: 3-12.
[http://dx.doi.org/10.1016/j.mrrev.2016.07.002] [PMID: 28528688]
[23]
Wang R, Pan W, Jin L, et al. Human papillomavirus vaccine against cervical cancer: Opportunity and challenge. Cancer Lett 2020; 471: 88-102.
[http://dx.doi.org/10.1016/j.canlet.2019.11.039] [PMID: 31812696]
[24]
Tommasino M. The human papillomavirus family and its role in carcinogenesis. Semin Cancer Biol 2014; 26: 13-21.
[http://dx.doi.org/10.1016/j.semcancer.2013.11.002] [PMID: 24316445]
[25]
Schellenbacher C, Roden RBS, Kirnbauer R. Developments in L2-based human papillomavirus (HPV) vaccines. Virus Res 2017; 231: 166-75.
[http://dx.doi.org/10.1016/j.virusres.2016.11.020] [PMID: 27889616]
[26]
Moody CA, Laimins LA. Human papillomavirus oncoproteins: Pathways to transformation. Nat Rev Cancer 2010; 10(8): 550-60.
[http://dx.doi.org/10.1038/nrc2886] [PMID: 20592731]
[27]
Pullos AN, Castilho RM, Squarize CH. HPV infection of the head and neck region and its stem cells. J Dent Res 2015; 94(11): 1532-43.
[http://dx.doi.org/10.1177/0022034515605456] [PMID: 26353884]
[28]
Handler MZ, Handler NS, Majewski S, Schwartz RA. Human papillomavirus vaccine trials and tribulations: Clinical perspectives. J Am Acad Dermatol 2015; 73(5): 743-56.
[http://dx.doi.org/10.1016/j.jaad.2015.05.040] [PMID: 26475534]
[29]
Buck CB, Pastrana DV, Lowy DR, Schiller JT. Efficient intracellular assembly of papillomaviral vectors. J Virol 2004; 78(2): 751-7.
[http://dx.doi.org/10.1128/JVI.78.2.751-757.2004] [PMID: 14694107]
[30]
Leder C, Kleinschmidt JA, Wiethe C, Müller M. Enhancement of capsid gene expression: Preparing the human papillomavirus type 16 major structural gene L1 for DNA vaccination purposes. J Virol 2001; 75(19): 9201-9.
[http://dx.doi.org/10.1128/JVI.75.19.9201-9209.2001] [PMID: 11533183]
[31]
Mouw JK, Ou G, Weaver VM. Extracellular matrix assembly: A multiscale deconstruction. Nat Rev Mol Cell Biol 2014; 15(12): 771-85.
[http://dx.doi.org/10.1038/nrm3902] [PMID: 25370693]
[32]
Esko JD, Lindahl U. Molecular diversity of heparan sulfate. J Clin Invest 2001; 108(2): 169-73.
[http://dx.doi.org/10.1172/JCI200113530] [PMID: 11457867]
[33]
Johnson KM, Kines RC, Roberts JN, Lowy DR, Schiller JT, Day PM. Role of heparan sulfate in attachment to and infection of the murine female genital tract by human papillomavirus. J Virol 2009; 83(5): 2067-74.
[http://dx.doi.org/10.1128/JVI.02190-08] [PMID: 19073722]
[34]
Dasgupta J, Bienkowska-Haba M, Ortega ME, et al. Structural basis of oligosaccharide receptor recognition by human papillomavirus. J Biol Chem 2011; 286(4): 2617-24.
[http://dx.doi.org/10.1074/jbc.M110.160184] [PMID: 21115492]
[35]
Richards KF, Mukherjee S, Bienkowska-Haba M, Pang J, Sapp M. Human papillomavirus species-specific interaction with the basement membrane-resident non-heparan sulfate receptor. Viruses 2014; 6(12): 4856-79.
[http://dx.doi.org/10.3390/v6124856] [PMID: 25490765]
[36]
Culp TD, Budgeon LR, Marinkovich MP, Meneguzzi G, Christensen ND. Keratinocyte-secreted laminin 5 can function as a transient receptor for human papillomaviruses by binding virions and transferring them to adjacent cells. J Virol 2006; 80(18): 8940-50.
[http://dx.doi.org/10.1128/JVI.00724-06] [PMID: 16940506]
[37]
Bienkowska-Haba M, Patel HD, Sapp M. Target cell cyclophilins facilitate human papillomavirus type 16 infection. PLoS Pathog 2009; 5(7): e1000524.
[http://dx.doi.org/10.1371/journal.ppat.1000524] [PMID: 19629175]
[38]
Day PM, Gambhira R, Roden RB, Lowy DR, Schiller JT. Mechanisms of human papillomavirus type 16 neutralization by l2 cross-neutralizing and l1 type-specific antibodies. J Virol 2008; 82(9): 4638-46.
[http://dx.doi.org/10.1128/JVI.00143-08] [PMID: 18305047]
[39]
Scheffer KD, Gawlitza A, Spoden GA, et al. Tetraspanin CD151 mediates papillomavirus type 16 endocytosis. J Virol 2013; 87(6): 3435-46.
[http://dx.doi.org/10.1128/JVI.02906-12] [PMID: 23302890]
[40]
Scheffer KD, Berditchevski F, Florin L. The tetraspanin CD151 in papillomavirus infection. Viruses 2014; 6(2): 893-908.
[http://dx.doi.org/10.3390/v6020893] [PMID: 24553111]
[41]
Spoden G, Freitag K, Husmann M, et al. Clathrin- and caveolin-independent entry of human papillomavirus type 16--involvement of tetraspanin-enriched microdomains (TEMs). PLoS One 2008; 3(10): e3313.
[http://dx.doi.org/10.1371/journal.pone.0003313] [PMID: 18836553]
[42]
Graham SV. The human papillomavirus replication cycle, and its links to cancer progression: A comprehensive review. Clin Sci (Lond) 2017; 131(17): 2201-21.
[http://dx.doi.org/10.1042/CS20160786] [PMID: 28798073]
[43]
LaFleur DW, Nardelli B, Tsareva T, et al. Interferon-kappa, a novel type I interferon expressed in human keratinocytes. J Biol Chem 2001; 276(43): 39765-71.
[http://dx.doi.org/10.1074/jbc.M102502200] [PMID: 11514542]
[44]
Chessa C, Bodet C, Jousselin C, Wehbe M, Lévêque N, Garcia M. Antiviral and immunomodulatory properties of antimicrobial peptides produced by human keratinocytes. Front Microbiol 2020; 11: 1155.
[http://dx.doi.org/10.3389/fmicb.2020.01155] [PMID: 32582097]
[45]
Li S, Labrecque S, Gauzzi MC, et al. The human papilloma virus (HPV)-18 E6 oncoprotein physically associates with Tyk2 and impairs Jak-STAT activation by interferon-alpha. Oncogene 1999; 18(42): 5727-37.
[http://dx.doi.org/10.1038/sj.onc.1202960] [PMID: 10523853]
[46]
Barnard P, Payne E, McMillan NAJ. The human papillomavirus E7 protein is able to inhibit the antiviral and anti-growth functions of interferon-α. Virology 2000; 277(2): 411-9.
[http://dx.doi.org/10.1006/viro.2000.0584] [PMID: 11080488]
[47]
Cicchini L, Westrich JA, Xu T, et al. Suppression of antitumor immune responses by human papillomavirus through epigenetic downregulation of CXCL14. MBio 2016; 7(3): e00270-16.
[http://dx.doi.org/10.1128/mBio.00270-16] [PMID: 27143385]
[48]
Deng S, Deng Q, Zhang Y, et al. Non-platelet-derived CXCL4 differentially regulates cytotoxic and regulatory T cells through CXCR3 to suppress the immune response to colon cancer. Cancer Lett 2019; 443: 1-12.
[http://dx.doi.org/10.1016/j.canlet.2018.11.017] [PMID: 30481563]
[49]
Artaza-Irigaray C, Molina-Pineda A, Aguilar-Lemarroy A, et al. E6/E7 and E6* from HPV16 and HPV18 upregulate IL-6 expression independently of p53 in Keratinocytes. Front Immunol 2019; 10: 1676.
[http://dx.doi.org/10.3389/fimmu.2019.01676] [PMID: 31396215]
[50]
Scott ML, Woodby BL, Ulicny J, et al. Human papillomavirus 16 e5 inhibits interferon signaling and supports episomal viral maintenance. J Virol 2020; 94(2): 94.
[http://dx.doi.org/10.1128/JVI.01582-19] [PMID: 31666385]
[51]
van der Pol Y, Mouliere F. Toward the early detection of cancer by decoding the epigenetic and environmental fingerprints of cell-free DNA. Cancer Cell 2019; 36(4): 350-68.
[http://dx.doi.org/10.1016/j.ccell.2019.09.003] [PMID: 31614115]
[52]
Raab-Traub N, Dittmer DP. Viral effects on the content and function of extracellular vesicles. Nat Rev Microbiol 2017; 15(9): 559-72.
[http://dx.doi.org/10.1038/nrmicro.2017.60] [PMID: 28649136]
[53]
Zhang J, Burn C, Young K, et al. Microparticles produced by human papillomavirus type 16 E7-expressing cells impair antigen presenting cell function and the cytotoxic T cell response. Sci Rep 2018; 8(1): 2373.
[http://dx.doi.org/10.1038/s41598-018-20779-2] [PMID: 29402982]
[54]
Guenat D, Hermetet F, Prétet JL, Mougin C. Exosomes and other extracellular vesicles in hpv transmission and carcinogenesis. Viruses 2017; 9(8): 211.
[http://dx.doi.org/10.3390/v9080211] [PMID: 28783104]
[55]
Chiantore MV, Mangino G, Iuliano M, et al. Human papillomavirus E6 and E7 oncoproteins affect the expression of cancer-related microRNAs: Additional evidence in HPV-induced tumorigenesis. J Cancer Res Clin Oncol 2016; 142(8): 1751-63.
[http://dx.doi.org/10.1007/s00432-016-2189-1] [PMID: 27300513]
[56]
Campo MS, Graham SV, Cortese MS, et al. HPV-16 E5 down-regulates expression of surface HLA class I and reduces recognition by CD8 T cells. Virology 2010; 407(1): 137-42.
[http://dx.doi.org/10.1016/j.virol.2010.07.044] [PMID: 20813390]
[57]
Miura S, Kawana K, Schust DJ, et al. CD1d, a sentinel molecule bridging innate and adaptive immunity, is downregulated by the human papillomavirus (HPV) E5 protein: A possible mechanism for immune evasion by HPV. J Virol 2010; 84(22): 11614-23.
[http://dx.doi.org/10.1128/JVI.01053-10] [PMID: 20810727]
[58]
Hubert P, Caberg JH, Gilles C, et al. E-cadherin-dependent adhesion of dendritic and Langerhans cells to keratinocytes is defective in cervical human papillomavirus-associated (pre)neoplastic lesions. J Pathol 2005; 206(3): 346-55.
[http://dx.doi.org/10.1002/path.1771] [PMID: 15852499]
[59]
Laurson J, Khan S, Chung R, Cross K, Raj K. Epigenetic repression of E-cadherin by human papillomavirus 16 E7 protein. Carcinogenesis 2010; 31(5): 918-26.
[http://dx.doi.org/10.1093/carcin/bgq027] [PMID: 20123756]
[60]
Lin D, Kouzy R, Abi Jaoude J, et al. Microbiome factors in HPV-driven carcinogenesis and cancers. PLoS Pathog 2020; 16(6): e1008524.
[http://dx.doi.org/10.1371/journal.ppat.1008524] [PMID: 32497113]
[61]
Wang X, Huang X, Zhang Y. Involvement of human papillomaviruses in cervical cancer. Front Microbiol 2018; 9: 2896.
[http://dx.doi.org/10.3389/fmicb.2018.02896] [PMID: 30546351]
[62]
Jiang B, Xue M. Correlation of E6 and E7 levels in high-risk HPV16 type cervical lesions with CCL20 and Langerhans cells. Genet Mol Res 2015; 14(3): 10473-81.
[http://dx.doi.org/10.4238/2015.September.8.8] [PMID: 26400278]
[63]
Barros MR Jr, de Melo CML, Barros MLCMGR, de Cássia Pereira de Lima R, de Freitas AC, Venuti A. Activities of stromal and immune cells in HPV-related cancers. J Exp Clin Cancer Res 2018; 37(1): 137.
[http://dx.doi.org/10.1186/s13046-018-0802-7] [PMID: 29976244]
[64]
Draghiciu O, Lubbers J, Nijman HW, Daemen T. Myeloid derived suppressor cells-An overview of combat strategies to increase immunotherapy efficacy. OncoImmunology 2015; 4(1): e954829.
[http://dx.doi.org/10.4161/21624011.2014.954829] [PMID: 25949858]
[65]
Weber R, Fleming V, Hu X, et al. Myeloid-derived suppressor cells hinder the anti-cancer activity of immune checkpoint inhibitors. Front Immunol 2018; 9: 1310.
[http://dx.doi.org/10.3389/fimmu.2018.01310] [PMID: 29942309]
[66]
Heine A, Held SAE, Schulte-Schrepping J, et al. Generation and functional characterization of MDSC-like cells. OncoImmunology 2017; 6(4): e1295203.
[http://dx.doi.org/10.1080/2162402X.2017.1295203] [PMID: 28507805]
[67]
Zhang J, Jin S, Li X, et al. Human papillomavirus type 16 disables the increased natural killer cells in early lesions of the cervix. J Immunol Res 2019; 2019: 9182979.
[http://dx.doi.org/10.1155/2019/9182979] [PMID: 31183395]
[68]
Ferns DM, Kema IP, Buist MR, Nijman HW, Kenter GG, Jordanova ES. Indoleamine-2,3-dioxygenase (IDO) metabolic activity is detrimental for cervical cancer patient survival. OncoImmunology 2015; 4(2): e981457.
[http://dx.doi.org/10.4161/2162402X.2014.981457] [PMID: 25949879]
[69]
Morrow MP, Kraynyak KA, Sylvester AJ, et al. Clinical and immunologic biomarkers for histologic regression of high-grade cervical dysplasia and clearance of hpv16 and hpv18 after immunotherapy. Clin Cancer Res 2018; 24(2): 276-94.
[http://dx.doi.org/10.1158/1078-0432.CCR-17-2335] [PMID: 29084917]
[70]
Maskey N, Thapa N, Maharjan M, et al. Infiltrating CD4 and CD8 lymphocytes in HPV infected uterine cervical milieu. Cancer Manag Res 2019; 11: 7647-55.
[http://dx.doi.org/10.2147/CMAR.S217264] [PMID: 31616181]
[71]
Pietras K, Pahler J, Bergers G, Hanahan D. Functions of paracrine PDGF signaling in the proangiogenic tumor stroma revealed by pharmacological targeting. PLoS Med 2008; 5(1): e19.
[http://dx.doi.org/10.1371/journal.pmed.0050019] [PMID: 18232728]
[72]
Chen R, Alvero AB, Silasi DA, Steffensen KD, Mor G. Cancers take their Toll--the function and regulation of Toll-like receptors in cancer cells. Oncogene 2008; 27(2): 225-33.
[http://dx.doi.org/10.1038/sj.onc.1210907] [PMID: 18176604]
[73]
D’Anna R, Le Buanec H, Bizzini B, et al. Human papillomavirus-16-E7 oncoprotein enhances the expression of adhesion molecules in cervical endothelial cells but not in human umbilical vein endothelial cells. J Hum Virol 2001; 4(2): 85-95.
[PMID: 11437318]
[74]
Füle T, Máthé M, Suba Z, et al. The presence of human papillomavirus 16 in neural structures and vascular endothelial cells. Virology 2006; 348(2): 289-96.
[http://dx.doi.org/10.1016/j.virol.2005.12.043] [PMID: 16499942]
[75]
Ilhan ZE, Łaniewski P, Thomas N, Roe DJ, Chase DM, Herbst-Kralovetz MM. Deciphering the complex interplay between microbiota, HPV, inflammation and cancer through cervicovaginal metabolic profiling. EBioMedicine 2019; 44: 675-90.
[http://dx.doi.org/10.1016/j.ebiom.2019.04.028] [PMID: 31027917]
[76]
Godoy-Vitorino F, Ortiz-Morales G, Romaguera J, Sanchez MM, Martinez-Ferrer M, Chorna N. Discriminating high-risk cervical human papilloma virus infections with urinary biomarkers via non-targeted gc-ms-based metabolomics. PLoS One 2018; 13(12): e0209936.
[http://dx.doi.org/10.1371/journal.pone.0209936] [PMID: 30592768]
[77]
Cruz-Gregorio A, Aranda-Rivera AK, Pedraza-Chaverri J. Human Papillomavirus-related cancers and mitochondria. Virus Res 2020; 286: 198016.
[http://dx.doi.org/10.1016/j.virusres.2020.198016] [PMID: 32445871]
[78]
Martínez-Ramírez I, Carrillo-García A, Contreras-Paredes A, Ortiz-Sánchez E, Cruz-Gregorio A, Lizano M. Regulation of cellular metabolism by high-risk human papillomaviruses. Int J Mol Sci 2018; 19(7): 1839.
[http://dx.doi.org/10.3390/ijms19071839] [PMID: 29932118]
[79]
Doorbar J. The papillomavirus life cycle. J Clin Virol 2005; 32(Suppl. 1): S7-S15.
[http://dx.doi.org/10.1016/j.jcv.2004.12.006] [PMID: 15753007]
[80]
Chow LT, Broker TR, Steinberg BM. The natural history of human papillomavirus infections of the mucosal epithelia. APMIS 2010; 118(6-7): 422-49.
[http://dx.doi.org/10.1111/j.1600-0463.2010.02625.x] [PMID: 20553526]
[81]
Stanley MA, Pett M. Papillomaviruses. In: Mahy BWJ, ter Meulen V, Eds. Wilson’s microbiology & microbial infections topley & virology. (10th ed.). Hoboken, NJ: Wiley-Blackwell 2007; pp. 448-72.
[82]
Ablasser A, Bauernfeind F, Hartmann G, Latz E, Fitzgerald KA, Hornung V. RIG-I-dependent sensing of poly(dA:dT) through the induction of an RNA polymerase III-transcribed RNA intermediate. Nat Immunol 2009; 10(10): 1065-72.
[http://dx.doi.org/10.1038/ni.1779] [PMID: 19609254]
[83]
Scott M, Nakagawa M, Moscicki AB. Cell-mediated immune response to human papillomavirus infection. Clin Diagn Lab Immunol 2001; 8(2): 209-20.
[http://dx.doi.org/10.1128/CDLI.8.2.209-220.2001] [PMID: 11238198]
[84]
Lebre MC, van der Aar AM, van Baarsen L, et al. Human keratinocytes express functional Toll-like receptor 3, 4, 5, and 9. J Invest Dermatol 2007; 127(2): 331-41.
[http://dx.doi.org/10.1038/sj.jid.5700530] [PMID: 17068485]
[85]
Karim R, Tummers B, Meyers C, et al. Human papillomavirus (HPV) upregulates the cellular deubiquitinase UCHL1 to suppress the keratinocyte’s innate immune response. PLoS Pathog 2013; 9(5): e1003384.
[http://dx.doi.org/10.1371/journal.ppat.1003384] [PMID: 23717208]
[86]
Hong S, Mehta KP, Laimins LA. Suppression of STAT-1 expression by human papillomaviruses is necessary for differentiation-dependent genome amplification and plasmid maintenance. J Virol 2011; 85(18): 9486-94.
[http://dx.doi.org/10.1128/JVI.05007-11] [PMID: 21734056]
[87]
Sunthamala N, Thierry F, Teissier S, et al. E2 proteins of high risk human papillomaviruses down-modulate STING and IFN-κ transcription in keratinocytes. PLoS One 2014; 9(3): e91473.
[http://dx.doi.org/10.1371/journal.pone.0091473] [PMID: 24614210]
[88]
Mota F, Rayment N, Chong S, Singer A, Chain B. The antigen-presenting environment in normal and human papillomavirus (HPV)-related premalignant cervical epithelium. Clin Exp Immunol 1999; 116(1): 33-40.
[http://dx.doi.org/10.1046/j.1365-2249.1999.00826.x] [PMID: 10209502]
[89]
Vivier E, Tomasello E, Baratin M, Walzer T, Ugolini S. Functions of natural killer cells. Nat Immunol 2008; 9(5): 503-10.
[http://dx.doi.org/10.1038/ni1582] [PMID: 18425107]
[90]
Vitale M, Cantoni C, Pietra G, Mingari MC, Moretta L. Effect of tumor cells and tumor microenvironment on NK-cell function. Eur J Immunol 2014; 44(6): 1582-92.
[http://dx.doi.org/10.1002/eji.201344272] [PMID: 24777896]
[91]
Garcia-Iglesias T, Del Toro-Arreola A, Albarran-Somoza B, et al. Low NKp30, NKp46 and NKG2D expression and reduced cytotoxic activity on NK cells in cervical cancer and precursor lesions. BMC Cancer 2009; 9: 186.
[http://dx.doi.org/10.1186/1471-2407-9-186] [PMID: 19531227]
[92]
Embgenbroich M, Burgdorf S. Current concepts of antigen cross-presentation. Front Immunol 2018; 9: 1643.
[http://dx.doi.org/10.3389/fimmu.2018.01643] [PMID: 30061897]
[93]
Blauvelt A, Katz SI, Udey MC. Human Langerhans cells express E-cadherin. J Invest Dermatol 1995; 104(2): 293-6.
[http://dx.doi.org/10.1111/1523-1747.ep12612830] [PMID: 7829887]
[94]
Schwarzenberger K, Udey MC. Contact allergens and epidermal proinflammatory cytokines modulate Langerhans cell E-cadherin expression in situ. J Invest Dermatol 1996; 106(3): 553-8.
[http://dx.doi.org/10.1111/1523-1747.ep12344019] [PMID: 8648193]
[95]
Bashaw AA, Leggatt GR, Chandra J, Tuong ZK, Frazer IH. Modulation of antigen presenting cell functions during chronic HPV infection. Papillomavirus Res 2017; 4: 58-65.
[http://dx.doi.org/10.1016/j.pvr.2017.08.002] [PMID: 29179871]
[96]
Bosch FX, Manos MM, Muñoz N, et al. Prevalence of human papillomavirus in cervical cancer: A worldwide perspective. International biological study on cervical cancer (IBSCC) Study Group. J Natl Cancer Inst 1995; 87(11): 796-802.
[http://dx.doi.org/10.1093/jnci/87.11.796] [PMID: 7791229]
[97]
Medzhitov R, Janeway CA Jr. Decoding the patterns of self and nonself by the innate immune system. Science 2002; 296(5566): 298-300.
[http://dx.doi.org/10.1126/science.1068883] [PMID: 11951031]
[98]
Yang X, Cheng Y, Li C. The role of TLRs in cervical cancer with HPV infection: A review. Signal Transduct Target Ther 2017; 2: 17055.
[http://dx.doi.org/10.1038/sigtrans.2017.55] [PMID: 29263932]
[99]
Hasan UA, Bates E, Takeshita F, et al. TLR9 expression and function is abolished by the cervical cancer-associated human papillomavirus type 16. J Immunol 2007; 178(5): 3186-97.
[http://dx.doi.org/10.4049/jimmunol.178.5.3186] [PMID: 17312167]
[100]
Kalali BN, Köllisch G, Mages J, et al. Double-stranded RNA induces an antiviral defense status in epidermal keratinocytes through TLR3-, PKR-, and MDA5/RIG-I-mediated differential signaling. J Immunol 2008; 181(4): 2694-704.
[http://dx.doi.org/10.4049/jimmunol.181.4.2694] [PMID: 18684960]
[101]
El-Omar EM, Ng MT, Hold GL. Polymorphisms in Toll-like receptor genes and risk of cancer. Oncogene 2008; 27(2): 244-52.
[http://dx.doi.org/10.1038/sj.onc.1210912] [PMID: 18176606]
[102]
Kawai T, Akira S. Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 2011; 34(5): 637-50.
[http://dx.doi.org/10.1016/j.immuni.2011.05.006] [PMID: 21616434]
[103]
Kerur N, Veettil MV, Sharma-Walia N, et al. IFI16 acts as a nuclear pathogen sensor to induce the inflammasome in response to Kaposi Sarcoma-associated herpesvirus infection. Cell Host Microbe 2011; 9(5): 363-75.
[http://dx.doi.org/10.1016/j.chom.2011.04.008] [PMID: 21575908]
[104]
Hornung V, Ablasser A, Charrel-Dennis M, et al. AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature 2009; 458(7237): 514-8.
[http://dx.doi.org/10.1038/nature07725] [PMID: 19158675]
[105]
Ludlow LE, Johnstone RW, Clarke CJ. The HIN-200 family: more than interferon-inducible genes? Exp Cell Res 2005; 308(1): 1-17.
[http://dx.doi.org/10.1016/j.yexcr.2005.03.032] [PMID: 15896773]
[106]
Reinholz M, Kawakami Y, Salzer S, et al. HPV16 activates the AIM2 inflammasome in keratinocytes. Arch Dermatol Res 2013; 305(8): 723-32.
[http://dx.doi.org/10.1007/s00403-013-1375-0] [PMID: 23764897]
[107]
Jakobsen MR, Bak RO, Andersen A. IFI16 senses DNA forms of the lentiviral replication cycle and controls HIV-1 replication. Proc Natl Acad Sci USA 2013; 110: E4571-80.
[108]
Stetson DB, Medzhitov R. Type I interferons in host defense. Immunity 2006; 25(3): 373-81.
[http://dx.doi.org/10.1016/j.immuni.2006.08.007] [PMID: 16979569]
[109]
Scott ME, Ma Y, Kuzmich L, Moscicki AB. Diminished IFN-gamma and IL-10 and elevated Foxp3 mRNA expression in the cervix are associated with CIN 2 or 3. Int J Cancer 2009; 124(6): 1379-83.
[http://dx.doi.org/10.1002/ijc.24117] [PMID: 19089920]
[110]
Song JY, Han JH, Song Y, Lee JH, Choi SY, Park YM. Epigallocatechin-3-gallate can prevent type 2 human papillomavirus E7 from suppressing interferon-stimulated genes. Int J Mol Sci 2021; 22(5): 2418.
[http://dx.doi.org/10.3390/ijms22052418] [PMID: 33670861]
[111]
Markiewski MM, DeAngelis RA, Benencia F, et al. Modulation of the antitumor immune response by complement. Nat Immunol 2008; 9(11): 1225-35.
[http://dx.doi.org/10.1038/ni.1655] [PMID: 18820683]
[112]
Ricklin D, Hajishengallis G, Yang K, Lambris JD. Complement: A key system for immune surveillance and homeostasis. Nat Immunol 2010; 11(9): 785-97.
[http://dx.doi.org/10.1038/ni.1923] [PMID: 20720586]
[113]
Markiewski MM, Lambris JD. The role of complement in inflammatory diseases from behind the scenes into the spotlight. Am J Pathol 2007; 171(3): 715-27.
[http://dx.doi.org/10.2353/ajpath.2007.070166] [PMID: 17640961]
[114]
Canales NA, Marina VM, Castro JS, et al. A1BG and C3 are overexpressed in patients with cervical intraepithelial neoplasia III. Oncol Lett 2014; 8(2): 939-47.
[http://dx.doi.org/10.3892/ol.2014.2195] [PMID: 25009667]
[115]
Stanley M. Immune responses to human papillomavirus. Vaccine 2006; 24(Suppl. 1): S16-22.
[http://dx.doi.org/10.1016/j.vaccine.2005.09.002] [PMID: 16219398]
[116]
Moerman-Herzog A, Nakagawa M. Early defensive mechanisms against human papillomavirus infection. Clin Vaccine Immunol 2015; 22(8): 850-7.
[http://dx.doi.org/10.1128/CVI.00223-15] [PMID: 26063238]
[117]
Azar KK, Tani M, Yasuda H, Sakai A, Inoue M, Sasagawa T. Increased secretion patterns of interleukin-10 and tumor necrosis factor-alpha in cervical squamous intraepithelial lesions. Hum Pathol 2004; 35(11): 1376-84.
[http://dx.doi.org/10.1016/j.humpath.2004.08.012] [PMID: 15668895]
[118]
Alves JJP, De Medeiros Fernandes TAA, De Araújo JMG, et al. Th17 response in patients with cervical cancer. Oncol Lett 2018; 16(5): 6215-27.
[http://dx.doi.org/10.3892/ol.2018.9481] [PMID: 30405758]
[119]
Tanaka A, Sakaguchi S. Regulatory T cells in cancer immunotherapy. Cell Res 2017; 27(1): 109-18.
[http://dx.doi.org/10.1038/cr.2016.151] [PMID: 27995907]
[120]
Stone SC, Rossetti RA, Lima AM, Lepique AP. HPV associated tumor cells control tumor microenvironment and leukocytosis in experimental models. Immun Inflamm Dis 2014; 2(2): 63-75.
[http://dx.doi.org/10.1002/iid3.21] [PMID: 25400927]
[121]
Bhairavabhotla RK, Verm V, Tongaonkar H, Shastri S, Dinshaw K, Chiplunkar S. Role of IL-10 in immune suppression in cervical cancer. Indian J Biochem Biophys 2007; 44(5): 350-6.
[PMID: 18341210]
[122]
Moir S, Fauci AS. B cells in HIV infection and disease. Nat Rev Immunol 2009; 9(4): 235-45.
[http://dx.doi.org/10.1038/nri2524] [PMID: 19319142]
[123]
Tang A, Dadaglio G, Oberkampf M, et al. B cells promote tumor progression in a mouse model of HPV-mediated cervical cancer. Int J Cancer 2016; 139(6): 1358-71.
[http://dx.doi.org/10.1002/ijc.30169] [PMID: 27130719]
[124]
Kim SS, Shen S, Miyauchi S, et al. B cells improve overall survival in HPV-associated squamous cell carcinomas and are activated by radiation and PD-1 blockade. Clin Cancer Res 2020; 26(13): 3345-59.
[http://dx.doi.org/10.1158/1078-0432.CCR-19-3211] [PMID: 32193227]
[125]
Rodríguez AC, Schiffman M, Herrero R, et al. Low risk of type-specific carcinogenic HPV re-appearance with subsequent cervical intraepithelial neoplasia grade 2/3. Int J Cancer 2012; 131(8): 1874-81.
[http://dx.doi.org/10.1002/ijc.27418] [PMID: 22213126]
[126]
Beachler DC, Jenkins G, Safaeian M, Kreimer AR, Wentzensen N. Natural acquired immunity against subsequent genital human papillomavirus infection: a systematic review and meta-analysis. J Infect Dis 2016; 213(9): 1444-54.
[http://dx.doi.org/10.1093/infdis/jiv753] [PMID: 26690341]
[127]
Combes JD, Pawlita M, Waterboer T, et al. Antibodies against high-risk human papillomavirus proteins as markers for invasive cervical cancer. Int J Cancer 2014; 135(10): 2453-61.
[http://dx.doi.org/10.1002/ijc.28888] [PMID: 24729277]
[128]
Zumbach K, Kisseljov F, Sacharova O, et al. Antibodies against oncoproteins E6 and E7 of human papillomavirus types 16 and 18 in cervical-carcinoma patients from Russia. Int J Cancer 2000; 85(3): 313-8.
[http://dx.doi.org/10.1002/(SICI)1097-0215(20000201)85:3<313::AID-IJC3>3.0.CO;2-W] [PMID: 10652419]
[129]
Ramezani A, Aghakhani A, Soleymani S, Bavand A, Bolhassani A. Significance of serum antibodies against HPV E7, Hsp27, Hsp20 and Hp91 in Iranian HPV-exposed women. BMC Infect Dis 2019; 19(1): 142.
[http://dx.doi.org/10.1186/s12879-019-3780-2] [PMID: 30755156]
[130]
Schiffman M, Doorbar J, Wentzensen N, et al. Carcinogenic human papillomavirus infection. Nat Rev Dis Primers 2016; 2: 16086.
[http://dx.doi.org/10.1038/nrdp.2016.86] [PMID: 27905473]
[131]
Stern PL. Immune control of human papillomavirus (HPV) associated anogenital disease and potential for vaccination. J Clin Virol 2005; 32(Suppl. 1): S72-81.
[http://dx.doi.org/10.1016/j.jcv.2004.12.005] [PMID: 15753015]
[132]
McBride AA, Warburton A. The role of integration in oncogenic progression of HPV-associated cancers. PLoS Pathog 2017; 13(4): e1006211.
[http://dx.doi.org/10.1371/journal.ppat.1006211] [PMID: 28384274]
[133]
Isaacson Wechsler E, Wang Q, Roberts I, et al. Reconstruction of human papillomavirus type 16-mediated early-stage neoplasia implicates E6/E7 deregulation and the loss of contact inhibition in neoplastic progression. J Virol 2012; 86(11): 6358-64.
[http://dx.doi.org/10.1128/JVI.07069-11] [PMID: 22457518]
[134]
Steinbach A, Riemer AB. Immune evasion mechanisms of human papillomavirus: An update. Int J Cancer 2018; 142(2): 224-9.
[http://dx.doi.org/10.1002/ijc.31027] [PMID: 28865151]
[135]
Wu J, Sun L, Chen X, et al. Cyclic GMP-AMP is an endogenous second messenger in innate immune signaling by cytosolic DNA. Science 2013; 339(6121): 826-30.
[http://dx.doi.org/10.1126/science.1229963] [PMID: 23258412]
[136]
Hasan UA, Zannetti C, Parroche P, et al. The human papillomavirus type 16 E7 oncoprotein induces a transcriptional repressor complex on the Toll-like receptor 9 promoter. J Exp Med 2013; 210(7): 1369-87.
[http://dx.doi.org/10.1084/jem.20122394] [PMID: 23752229]
[137]
Senba M, Buziba N, Mori N, et al. Human papillomavirus infection induces NF-κB activation in cervical cancer: A comparison with penile cancer. Oncol Lett 2011; 2(1): 65-8.
[http://dx.doi.org/10.3892/ol.2010.207] [PMID: 22870130]
[138]
Sieker F, Straatsma TP, Springer S, Zacharias M. Differential tapasin dependence of MHC class I molecules correlates with conformational changes upon peptide dissociation: A molecular dynamics simulation study. Mol Immunol 2008; 45(14): 3714-22.
[http://dx.doi.org/10.1016/j.molimm.2008.06.009] [PMID: 18639935]
[139]
Steinbach A, Winter J, Reuschenbach M, et al. ERAP1 overexpression in HPV-induced malignancies: A possible novel immune evasion mechanism. OncoImmunology 2017; 6(7): e1336594.
[http://dx.doi.org/10.1080/2162402X.2017.1336594] [PMID: 28811980]
[140]
Evans M, Borysiewicz LK, Evans AS, et al. Antigen processing defects in cervical carcinomas limit the presentation of a CTL epitope from human papillomavirus 16 E6. J Immunol 2001; 167(9): 5420-8.
[http://dx.doi.org/10.4049/jimmunol.167.9.5420] [PMID: 11673561]
[141]
Hasim A, Abudula M, Aimiduo R, et al. Post-transcriptional and epigenetic regulation of antigen processing machinery (APM) components and HLA-I in cervical cancers from Uighur women. PLoS One 2012; 7(9): e44952.
[http://dx.doi.org/10.1371/journal.pone.0044952] [PMID: 23024775]
[142]
Heath WR, Carbone FR. The skin-resident and migratory immune system in steady state and memory: innate lymphocytes, dendritic cells and T cells. Nat Immunol 2013; 14(10): 978-85.
[http://dx.doi.org/10.1038/ni.2680] [PMID: 24048119]
[143]
Georgopoulos NT, Proffitt JL, Blair GE. Transcriptional regulation of the major histocompatibility complex (MHC) class I heavy chain, TAP1 and LMP2 genes by the human papillomavirus (HPV) type 6b, 16 and 18 E7 oncoproteins. Oncogene 2000; 19(42): 4930-5.
[http://dx.doi.org/10.1038/sj.onc.1203860] [PMID: 11039910]
[144]
Fausch SC, Da Silva DM, Rudolf MP, Kast WM. Human papillomavirus virus-like particles do not activate Langerhans cells: A possible immune escape mechanism used by human papillomaviruses. J Immunol 2002; 169(6): 3242-9.
[http://dx.doi.org/10.4049/jimmunol.169.6.3242] [PMID: 12218143]
[145]
Mantovani A, Sica A, Allavena P, Garlanda C, Locati M. Tumor-associated macrophages and the related myeloid-derived suppressor cells as a paradigm of the diversity of macrophage activation. Hum Immunol 2009; 70(5): 325-30.
[http://dx.doi.org/10.1016/j.humimm.2009.02.008] [PMID: 19236898]
[146]
Lepique AP, Daghastanli KR, Cuccovia IM, Villa LL. HPV16 tumor associated macrophages suppress antitumor T cell responses. Clin Cancer Res 2009; 15(13): 4391-400.
[http://dx.doi.org/10.1158/1078-0432.CCR-09-0489] [PMID: 19549768]
[147]
Yim EK, Park JS. The role of HPV E6 and E7 oncoproteins in HPV-associated cervical carcinogenesis. Cancer Res Treat 2005; 37(6): 319-24.
[http://dx.doi.org/10.4143/crt.2005.37.6.319] [PMID: 19956366]
[148]
Senba M, Mori N. Mechanisms of virus immune evasion lead to development from chronic inflammation to cancer formation associated with human papillomavirus infection. Oncol Rev 2012; 6(2): e17.
[http://dx.doi.org/10.4081/oncol.2012.e17] [PMID: 25992215]
[149]
Patel D, Incassati A, Wang N, McCance DJ. Human papillomavirus type 16 E6 and E7 cause polyploidy in human keratinocytes and up-regulation of G2-M-phase proteins. Cancer Res 2004; 64(4): 1299-306.
[http://dx.doi.org/10.1158/0008-5472.CAN-03-2917] [PMID: 14973072]
[150]
zur Hausen H. Papillomaviruses and cancer: From basic studies to clinical application. Nat Rev Cancer 2002; 2(5): 342-50.
[http://dx.doi.org/10.1038/nrc798] [PMID: 12044010]
[151]
Nguyen DX, Westbrook TF, McCance DJ. Human papillomavirus type 16 E7 maintains elevated levels of the cdc25A tyrosine phosphatase during deregulation of cell cycle arrest. J Virol 2002; 76(2): 619-32.
[http://dx.doi.org/10.1128/JVI.76.2.619-632.2002] [PMID: 11752153]
[152]
Thomas M, Pim D, Banks L. The role of the E6-p53 interaction in the molecular pathogenesis of HPV. Oncogene 1999; 18(53): 7690-700.
[http://dx.doi.org/10.1038/sj.onc.1202953] [PMID: 10618709]
[153]
Garnett TO, Filippova M, Duerksen-Hughes PJ. Accelerated degradation of FADD and procaspase 8 in cells expressing human papilloma virus 16 E6 impairs TRAIL-mediated apoptosis. Cell Death Differ 2006; 13(11): 1915-26.
[http://dx.doi.org/10.1038/sj.cdd.4401886] [PMID: 16528386]
[154]
Wilson VG, West M, Woytek K, Rangasamy D. Papillomavirus E1 proteins: Form, function, and features. Virus Genes 2002; 24(3): 275-90.
[http://dx.doi.org/10.1023/A:1015336817836] [PMID: 12086149]
[155]
Stenlund A. E1 initiator DNA binding specificity is unmasked by selective inhibition of non-specific DNA binding. EMBO J 2003; 22(4): 954-63.
[http://dx.doi.org/10.1093/emboj/cdg091] [PMID: 12574131]
[156]
Enemark EJ, Joshua-Tor L. Mechanism of DNA translocation in a replicative hexameric helicase. Nature 2006; 442(7100): 270-5.
[http://dx.doi.org/10.1038/nature04943] [PMID: 16855583]
[157]
Titolo S, Brault K, Majewski J, White PW, Archambault J. Characterization of the minimal DNA binding domain of the human papillomavirus e1 helicase: Fluorescence anisotropy studies and characterization of a dimerization-defective mutant protein. J Virol 2003; 77(9): 5178-91.
[http://dx.doi.org/10.1128/JVI.77.9.5178-5191.2003] [PMID: 12692220]
[158]
Morin G, Fradet-Turcotte A, Di Lello P, Bergeron-Labrecque F, Omichinski JG, Archambault J. A conserved amphipathic helix in the N-terminal regulatory region of the papillomavirus E1 helicase is required for efficient viral DNA replication. J Virol 2011; 85(11): 5287-300.
[http://dx.doi.org/10.1128/JVI.01829-10] [PMID: 21450828]
[159]
Chen G, Stenlund A. The E1 initiator recognizes multiple overlapping sites in the papillomavirus origin of DNA replication. J Virol 2001; 75(1): 292-302.
[http://dx.doi.org/10.1128/JVI.75.1.292-302.2001] [PMID: 11119599]
[160]
Lentz MR, Stevens SM Jr, Raynes J, Elkhoury N. A phosphorylation map of the bovine papillomavirus E1 helicase. Virol J 2006; 3: 13.
[http://dx.doi.org/10.1186/1743-422X-3-13] [PMID: 16524476]
[161]
Fujii T, Austin D, Guo D, et al. Peptides inhibitory for the transcriptional regulatory function of human papillomavirus E2. Clin Cancer Res 2003; 9(14): 5423-8.
[PMID: 14614029]
[162]
Kantang W, Chunsrivirot S, Muangsin N, Poovorawan Y, Krusong K. Design of peptides as inhibitors of human papillomavirus 16 transcriptional regulator E1-E2. Chem Biol Drug Des 2016; 88(4): 475-84.
[http://dx.doi.org/10.1111/cbdd.12790] [PMID: 27203784]
[163]
Deng W, Lin BY, Jin G, et al. Cyclin/CDK regulates the nucleocytoplasmic localization of the human papillomavirus E1 DNA helicase. J Virol 2004; 78(24): 13954-65.
[http://dx.doi.org/10.1128/JVI.78.24.13954-13965.2004] [PMID: 15564503]
[164]
Ziegert C, Wentzensen N, Vinokurova S, et al. A comprehensive analysis of HPV integration loci in anogenital lesions combining transcript and genome-based amplification techniques. Oncogene 2003; 22(25): 3977-84.
[http://dx.doi.org/10.1038/sj.onc.1206629] [PMID: 12813471]
[165]
Hancock G, Hellner K, Dorrell L. Therapeutic HPV vaccines. Best Practice and Research. Clin Obstet Gynecol 2018; 47: 59-72.
[166]
Schuck S, Ruse C, Stenlund A. CK2 phosphorylation inactivates DNA binding by the papillomavirus E1 and E2 proteins. J Virol 2013; 87(13): 7668-79.
[http://dx.doi.org/10.1128/JVI.00345-13] [PMID: 23637413]
[167]
Stenlund A. Initiation of DNA replication: Lessons from viral initiator proteins. Nat Rev Mol Cell Biol 2003; 4(10): 777-85.
[http://dx.doi.org/10.1038/nrm1226] [PMID: 14504622]
[168]
Moon RT, Kohn AD, De Ferrari GV, Kaykas A. WNT and beta-catenin signalling: Diseases and therapies. Nat Rev Genet 2004; 5(9): 691-701.
[http://dx.doi.org/10.1038/nrg1427] [PMID: 15372092]
[169]
Yamada T, Takaoka AS, Naishiro Y, et al. Transactivation of the multidrug resistance 1 gene by T-cell factor 4/beta-catenin complex in early colorectal carcinogenesis. Cancer Res 2000; 60(17): 4761-6.
[PMID: 10987283]
[170]
Manzo-Merino J, Contreras-Paredes A, Vázquez-Ulloa E, Rocha-Zavaleta L, Fuentes-Gonzalez AM, Lizano M. The role of signaling pathways in cervical cancer and molecular therapeutic targets. Arch Med Res 2014; 45(7): 525-39.
[http://dx.doi.org/10.1016/j.arcmed.2014.10.008] [PMID: 25450584]
[171]
Chen R, Alvero AB, Silasi DA, Mor G. Inflammation, cancer and chemoresistance: Taking advantage of the toll-like receptor signaling pathway. Am J Reprod Immunol 2007; 57(2): 93-107.
[http://dx.doi.org/10.1111/j.1600-0897.2006.00441.x] [PMID: 17217363]
[172]
McCain J. The MAPK (ERK) Pathway: Investigational combinations for the treatment of BRAF-mutated metastatic melanoma. P&T 2013; 38(2): 96-108.
[PMID: 23599677]
[173]
Menges CW, Baglia LA, Lapoint R, McCance DJ. Human papillomavirus type 16 E7 up-regulates AKT activity through the retinoblastoma protein. Cancer Res 2006; 66(11): 5555-9.
[http://dx.doi.org/10.1158/0008-5472.CAN-06-0499] [PMID: 16740689]
[174]
McMurray HR, McCance DJ. Human papillomavirus type 16 E6 activates TERT gene transcription through induction of c-Myc and release of USF-mediated repression. J Virol 2003; 77(18): 9852-61.
[http://dx.doi.org/10.1128/JVI.77.18.9852-9861.2003] [PMID: 12941894]
[175]
Polivka J Jr, Janku F. Molecular targets for cancer therapy in the PI3K/AKT/mTOR pathway. Pharmacol Ther 2014; 142(2): 164-75.
[http://dx.doi.org/10.1016/j.pharmthera.2013.12.004] [PMID: 24333502]
[176]
Bernard F, Krejci A, Housden B, Adryan B, Bray SJ. Specificity of Notch pathway activation: Twist controls the transcriptional output in adult muscle progenitors. Development 2010; 137(16): 2633-42.
[http://dx.doi.org/10.1242/dev.053181] [PMID: 20610485]
[177]
Tsai JH, Yang J. Epithelial-mesenchymal plasticity in carcinoma metastasis. Genes Dev 2013; 27(20): 2192-206.
[http://dx.doi.org/10.1101/gad.225334.113] [PMID: 24142872]
[178]
Al Moustafa AE, Achkhar A, Yasmeen A. EGF-receptor signaling and epithelial-mesenchymal transition in human carcinomas. Front Biosci (Schol Ed) 2012; 4: 671-84.
[http://dx.doi.org/10.2741/s292] [PMID: 22202084]
[179]
Jung YS, Kato I, Kim HR. A novel function of HPV16-E6/E7 in epithelial-mesenchymal transition. Biochem Biophys Res Commun 2013; 435(3): 339-44.
[http://dx.doi.org/10.1016/j.bbrc.2013.04.060] [PMID: 23628416]
[180]
Zhang D, Zhou XH, Zhang J, et al. Propofol promotes cell apoptosis via inhibiting HOTAIR mediated mTOR pathway in cervical cancer. Biochem Biophys Res Commun 2015; 468(4): 561-7.
[http://dx.doi.org/10.1016/j.bbrc.2015.10.129] [PMID: 26523512]
[181]
Chang H, Shyu KG, Lin S, et al. The plasminogen activator inhibitor-1 gene is induced by cell adhesion through the MEK/ERK pathway. J Biomed Sci 2003; 10(6 Pt 2): 738-45.
[http://dx.doi.org/10.1007/BF02256326] [PMID: 14631113]
[182]
Branca M, Ciotti M, Santini D, et al. Activation of the ERK/MAP kinase pathway in cervical intraepithelial neoplasia is related to grade of the lesion but not to high-risk human papillomavirus, virus clearance, or prognosis in cervical cancer. Am J Clin Pathol 2004; 122(6): 902-11.
[http://dx.doi.org/10.1309/VQXFT880JXC7QD2W] [PMID: 15539382]
[183]
Song ZC, Ding L, Ren ZY, et al. Effects of Src on cervical cancer cells proliferation and apoptosis through ERK signal transduction pathway. Zhonghua Liu Xing Bing Xue Za Zhi 2017; 38(9): 1246-51.
[PMID: 28910941]
[184]
Liu F, Lin B, Liu X, et al. ERK signaling pathway is involved in hpv-16 e6 but not e7 oncoprotein-induced hif-1α protein accumulation in nsclc cells. Oncol Res 2016; 23(3): 109-18.
[http://dx.doi.org/10.3727/096504015X14496932933610] [PMID: 26931433]
[185]
Bauknecht T, Shi Y. Overexpression of C/EBPbeta represses human papillomavirus type 18 upstream regulatory region activity in HeLa cells by interfering with the binding of TATA-binding protein. J Virol 1998; 72(3): 2113-24.
[http://dx.doi.org/10.1128/JVI.72.3.2113-2124.1998] [PMID: 9499067]
[186]
Guifen L, Fachun W, Enliang S, Xiaomu L, Xiuwen T, Zhenshan L. Effects of chromium picolinate supplementation on the growth, carcass quality and gene expression of beef during the finishing period. Mol Biol Rep 2011; 38(7): 4469-74.
[http://dx.doi.org/10.1007/s11033-010-0576-2] [PMID: 21161406]
[187]
Ojesina AI, Lichtenstein L, Freeman SS, et al. Landscape of genomic alterations in cervical carcinomas. Nature 2014; 506(7488): 371-5.
[http://dx.doi.org/10.1038/nature12881] [PMID: 24390348]
[188]
Brand TM, Iida M, Corrigan KL, et al. The receptor tyrosine kinase AXL mediates nuclear translocation of the epidermal growth factor receptor. Sci Signal 2017; 10(460): eaag1064.
[http://dx.doi.org/10.1126/scisignal.aag1064] [PMID: 28049763]
[189]
Soto U, Denk C, Finzer P, Hutter KJ, zur Hausen H, Rösl F. Genetic complementation to non-tumorigenicity in cervical-carcinoma cells correlates with alterations in AP-1 composition. Int J Cancer 2000; 86(6): 811-7.
[http://dx.doi.org/10.1002/(SICI)1097-0215(20000615)86:6<811::AID-IJC9>3.0.CO;2-J] [PMID: 10842195]
[190]
Dhandapani KM, Mahesh VB, Brann DW. Curcumin suppresses growth and chemoresistance of human glioblastoma cells via AP-1 and NFkappaB transcription factors. J Neurochem 2007; 102(2): 522-38.
[http://dx.doi.org/10.1111/j.1471-4159.2007.04633.x] [PMID: 17596214]
[191]
Tyagi A, Vishnoi K, Kaur H, et al. Cervical cancer stem cells manifest radioresistance: Association with upregulated AP-1 activity. Sci Rep 2017; 7(1): 4781.
[http://dx.doi.org/10.1038/s41598-017-05162-x] [PMID: 28684765]
[192]
Mishra A, Bharti AC, Varghese P, Saluja D, Das BC. Differential expression and activation of NF-kappaB family proteins during oral carcinogenesis: Role of high risk human papillomavirus infection. Int J Cancer 2006; 119(12): 2840-50.
[http://dx.doi.org/10.1002/ijc.22262] [PMID: 16998793]
[193]
Chen CL, Hsieh FC, Lieblein JC, et al. Stat3 activation in human endometrial and cervical cancers. Br J Cancer 2007; 96(4): 591-9.
[http://dx.doi.org/10.1038/sj.bjc.6603597] [PMID: 17311011]
[194]
Senba M, Mori N, Fujita S, et al. Relationship among human papillomavirus infection, p16(INK4a), p53 and NF-κB activation in penile cancer from northern Thailand. Oncol Lett 2010; 1(4): 599-603.
[http://dx.doi.org/10.3892/ol_00000106] [PMID: 22966350]
[195]
Senba M, Mori N, Wada A, et al. Human papillomavirus genotypes in penile cancers from Japanese patients and HPV-induced NF-κB activation. Oncol Lett 2010; 1(2): 267-72.
[http://dx.doi.org/10.3892/ol_00000047] [PMID: 22966292]
[196]
Havard L, Rahmouni S, Boniver J, Delvenne P. High levels of p105 (NFKB1) and p100 (NFKB2) proteins in HPV16-transformed keratinocytes: Role of E6 and E7 oncoproteins. Virology 2005; 331(2): 357-66.
[http://dx.doi.org/10.1016/j.virol.2004.10.030] [PMID: 15629778]
[197]
Ferreira AR, Ramalho AC, Marques M, Ribeiro D. The interplay between antiviral signalling and carcinogenesis in human papillomavirus infections. Cancers (Basel) 2020; 12(3): 646.
[http://dx.doi.org/10.3390/cancers12030646] [PMID: 32164347]
[198]
Antonsson A, Payne E, Hengst K, McMillan NAJ. The human papillomavirus type 16 E7 protein binds human interferon regulatory factor-9 via a novel PEST domain required for transformation. J Interferon Cytokine Res 2006; 26(7): 455-61.
[http://dx.doi.org/10.1089/jir.2006.26.455] [PMID: 16800784]
[199]
Chang YE, Laimins LA. Microarray analysis identifies interferon-inducible genes and Stat-1 as major transcriptional targets of human papillomavirus type 31. J Virol 2000; 74(9): 4174-82.
[http://dx.doi.org/10.1128/JVI.74.9.4174-4182.2000] [PMID: 10756030]
[200]
Reiser J, Hurst J, Voges M, et al. High-risk human papillomaviruses repress constitutive kappa interferon transcription via E6 to prevent pathogen recognition receptor and antiviral-gene expression. J Virol 2011; 85(21): 11372-80.
[http://dx.doi.org/10.1128/JVI.05279-11] [PMID: 21849431]
[201]
Hebner CM, Wilson R, Rader J, Bidder M, Laimins LA. Human papillomaviruses target the double-stranded RNA protein kinase pathway. J Gen Virol 2006; 87(Pt 11): 3183-93.
[http://dx.doi.org/10.1099/vir.0.82098-0] [PMID: 17030851]
[202]
Pacini L, Savini C, Ghittoni R, et al. Downregulation of toll-like receptor 9 expression by beta human papillomavirus 38 and implications for cell cycle control. J Virol 2015; 89(22): 11396-405.
[http://dx.doi.org/10.1128/JVI.02151-15] [PMID: 26339055]
[203]
Burgers WA, Blanchon L, Pradhan S, de Launoit Y, Kouzarides T, Fuks F. Viral oncoproteins target the DNA methyltransferases. Oncogene 2007; 26(11): 1650-5.
[http://dx.doi.org/10.1038/sj.onc.1209950] [PMID: 16983344]
[204]
Takeuchi O, Akira S. Pattern recognition receptors and inflammation. Cell 2010; 140(6): 805-20.
[http://dx.doi.org/10.1016/j.cell.2010.01.022] [PMID: 20303872]
[205]
White PW, Faucher AM, Massariol MJ, et al. Biphenylsulfonacetic acid inhibitors of the human papillomavirus type 6 E1 helicase inhibit ATP hydrolysis by an allosteric mechanism involving tyrosine 486. Antimicrob Agents Chemother 2005; 49(12): 4834-42.
[http://dx.doi.org/10.1128/AAC.49.12.4834-4842.2005] [PMID: 16304143]
[206]
Be X, Hong Y, Wei J, Androphy EJ, Chen JJ, Baleja JD. Solution structure determination and mutational analysis of the papillomavirus E6 interacting peptide of E6AP. Biochemistry 2001; 40(5): 1293-9.
[http://dx.doi.org/10.1021/bi0019592] [PMID: 11170455]
[207]
Baleja JD, Cherry JJ, Liu Z, et al. Identification of inhibitors to papillomavirus type 16 E6 protein based on three-dimensional structures of interacting proteins. Antiviral Res 2006; 72(1): 49-59.
[http://dx.doi.org/10.1016/j.antiviral.2006.03.014] [PMID: 16690141]
[208]
Longworth MS, 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 2004; 78(7): 3533-41.
[http://dx.doi.org/10.1128/JVI.78.7.3533-3541.2004] [PMID: 15016876]
[209]
Beadle JR, Valiaeva N, Yang G, et al. Synthesis and antiviral evaluation of octadecyloxyethyl benzyl 9-[(2-phosphonomethoxy)ethyl]guanine (ODE-BN-PMEG), a potent inhibitor of transient HPV DNA amplification. J Med Chem 2016; 59(23): 10470-8.
[http://dx.doi.org/10.1021/acs.jmedchem.6b00659] [PMID: 27933957]
[210]
Finzer P, Ventz R, Kuntzen C, Seibert N, Soto U, Rösl F. Growth arrest of HPV-positive cells after histone deacetylase inhibition is independent of E6/E7 oncogene expression. Virology 2002; 304(2): 265-73.
[http://dx.doi.org/10.1006/viro.2002.1667] [PMID: 12504567]
[211]
Gomez-Gutierrez JG, Elpek KG, Montes de Oca-Luna R, Shirwan H, Sam Zhou H, McMasters KM. Vaccination with an adenoviral vector expressing calreticulin-human papillomavirus 16 E7 fusion protein eradicates E7 expressing established tumors in mice. Cancer Immunol Immunother 2007; 56(7): 997-1007.
[http://dx.doi.org/10.1007/s00262-006-0247-2] [PMID: 17146630]
[212]
Kenter GG, Welters MJ, Valentijn AR, et al. Vaccination against HPV-16 oncoproteins for vulvar intraepithelial neoplasia. N Engl J Med 2009; 361(19): 1838-47.
[http://dx.doi.org/10.1056/NEJMoa0810097] [PMID: 19890126]
[213]
Waters NJ, Waterfield CJ, Farrant RD, Holmes E, Nicholson JK. Integrated metabonomic analysis of bromobenzene-induced novel hepatic 5-oxoprolinosis. J Proteome Res 2006; 5: 1448-59.
[http://dx.doi.org/10.1021/pr060024q] [PMID: 16739996]
[214]
Putri SP, Yamamoto S, Tsugawa H, Fukusaki E. Current metabolomics: Technological advances. J Biosci Bioeng 2013; 116(1): 9-16.
[http://dx.doi.org/10.1016/j.jbiosc.2013.01.004] [PMID: 23466298]
[215]
Zhang AH, Sun H, Qiu S, Wang XJ. NMR-based metabolomics coupled with pattern recognition methods in biomarker discovery and disease diagnosis. Magn Reson Chem 2013; 51(9): 549-56.
[http://dx.doi.org/10.1002/mrc.3985] [PMID: 23828598]
[216]
Emwas AH, Roy R, McKay RT, et al. NMR spectroscopy for metabolomics research. Metabolites 2019; 9(7): 123.
[http://dx.doi.org/10.3390/metabo9070123] [PMID: 31252628]
[217]
Emwas AH, Szczepski K, Poulson BG, et al. NMR as a “gold standard” method in drug design and discovery. Molecules 2020; 25(20): 4597.
[http://dx.doi.org/10.3390/molecules25204597] [PMID: 33050240]
[218]
Di Girolamo F, Lante I, Muraca M, Putignani L. The role of mass spectrometry in the “omics” era. Curr Org Chem 2013; 17(23): 2891-905.
[http://dx.doi.org/10.2174/1385272817888131118162725] [PMID: 24376367]

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