Abstract
Human papillomavirus (HPV) cancers are expected to be major global health concerns in the upcoming decades. The growth of HPV-positive cancer cells depends on the consistent expression of oncoprotein which has been poorly taken into account in the cellular communication. Among them, E6/E7 oncoproteins are attractive therapeutic targets as their inhibition rapidly leads to the onset of aging in HPV-positive cancer cells. This cellular response is associated with the regeneration of p53, pRb anti-proliferative proteins as well as the mTOR signaling pathway; hence, the identification of involved and application of E6/E7 inhibitors can lead to new therapeutic strategies. In the present review, we focused on the pathogenicity of E6/E7 Proteins of human papillomavirus and their roles associated with the cervical cancer.
Keywords: Human papillomavirus, cervical cancer, E6/E7 proteins, oncoprotein, cancer cells, pathogenicity.
Graphical Abstract
[1]
de Martel, C.; Ferlay, J.; Franceschi, S.; Vignat, J.; Bray, F.; Forman, D.; Plummer, M. Global burden of cancers attributable to infections in 2008: a review and synthetic analysis. Lancet Oncol., 2012, 13(6), 607-615.
[2]
Forman, D.; de Martel, C.; Lacey, C.J.; Soerjomataram, I.; Lortet-Tieulent, J.; Bruni, L.; Vignat, J.; Ferlay, J.; Bray, F.; Plummer, M.; Franceschi, S. Global burden of human papillomavirus and related diseases. Vaccine, 2012, 30(Suppl. 5), F12-F23.
[3]
Castle, P.E.; Jeronimo, J.; Temin, S.; Shastri, S.S. Screening to Prevent Invasive Cervical Cancer: ASCO Resource-Stratified Clinical Practice Guideline. J. Clin. Oncol., 2017, 35(11), 1250-1252.
[4]
Agorastos, T.; Chatzistamatiou, K.; Katsamagkas, T.; Koliopoulos, G.; Daponte, A.; Constantinidis, T.; Constantinidis, T.C. HERMES study group. Primary screening for cervical cancer based on high-risk human papillomavirus (HPV) detection and HPV 16 and HPV 18 genotyping, in comparison to cytology. PLoS One, 2015, 10(3), e0119755.
[5]
Chen, W.; Zheng, R.; Zeng, H.; Zhang, S.; He, J. Annual report on status of cancer in China, 2011. Chin. J. Cancer Res., 2015, 27(1), 2-12.
[6]
Burroni, E.; Sani, C.; Bisanzi, S.; Ocello, C. HPV primary test in the cervical cancer screening: reproducibility assessment and investigation on cytological outcome of Hybrid Capture 2 borderline samples. Epidemiol. Prev., 2016, 40(3-4), 164-170.
[7]
Network, C.G.A.R. Integrated genomic and molecular characterization of cervical cancer. Nature, 2017, 543(7645), 378-384.
[8]
Yuan, H.; Krawczyk, E.; Blancato, J.; Albanese, C.; Zhou, D.; Wang, N.; Paul, S.; Alkhilaiwi, F.; Palechor-Ceron, N.; Dakic, A.; Fang, S.; Choudhary, S.; Hou, T.W.; Zheng, Y.L.; Haddad, B.R.; Usuda, Y.; Hartmann, D.; Symer, D.; Gillison, M.; Agarwal, S.; Wangsa, D.; Ried, T.; Liu, X.; Schlegel, R. HPV positive neuroendocrine cervical cancer cells are dependent on Myc but not E6/E7 viral oncogenes. Sci. Rep., 2017, 7, 45617.
[9]
Yu, L. Deletion of HPV18 E6 and E7 genes using dual sgRNA-directed CRISPR/Cas9 inhibits growth of cervical cancer cells. Int. J. Clin. Exp. Med., 2017, 10(6), 9206-9213.
[10]
Hawley-Nelson, P.; Vousden, K.H.; Hubbert, N.L.; Lowy, D.R.; Schiller, J.T. HPV16 E6 and E7 proteins cooperate to immortalize human foreskin keratinocytes. EMBO J., 1989, 8(12), 3905-3910.
[11]
Hildesheim, A. Impact of human papillomavirus (HPV) 16 and 18
vaccination on prevalent infections and rates of cervical lesions after
excisional treatment Am. J. Obstet. Gynecol, 2016. 215, p.
(5)12. e1-212. e15.
[12]
Serrano, B.; de Sanjosé, S.; Tous, S.; Quiros, B.; Muñoz, N.; Bosch, X.; Alemany, L. Human papillomavirus genotype attribution for HPVs 6, 11, 16, 18, 31, 33, 45, 52 and 58 in female anogenital lesions. Eur. J. Cancer, 2015, 51(13), 1732-1741.
[13]
Taghizadeh, E. Distribution of human papillomavirus genotypes
among women in Mashhad, Iran; Intervirology, 2017.
[14]
DiGiuseppe, S.; Bienkowska-Haba, M.; Sapp, M. Human papillomavirus entry: hiding in a bubble. J. Virol., 2016, p. JVI. 01065-16.,
[15]
Xu, B.; Chotewutmontri, S.; Wolf, S.; Klos, U.; Schmitz, M.; Dürst, M.; Schwarz, E. Multiplex identification of human papillomavirus 16 DNA integration sites in cervical carcinomas. PLoS One, 2013, 8(6), e66693.
[16]
Doorbar, J.; Quint, W.; Banks, L.; Bravo, I.G.; Stoler, M.; Broker, T.R.; Stanley, M.A. The biology and life-cycle of human papillomaviruses. Vaccine, 2012, 30(Suppl. 5), F55-F70.
[17]
McBride, A.A. Mechanisms and strategies of papillomavirus replication. Biol. Chem., 2017, 398(8), 919-927.
[18]
Galloway, D.A.; Laimins, L.A. Human papillomaviruses: shared and distinct pathways for pathogenesis. Curr. Opin. Virol., 2015, 14, 87-92.
[19]
Groves, I.J.; Coleman, N. Pathogenesis of human papillomavirus-associated mucosal disease. J. Pathol., 2015, 235(4), 527-538.
[20]
Moody, C.A.; Laimins, L.A. Human papillomavirus oncoproteins: pathways to transformation. Nat. Rev. Cancer, 2010, 10(8), 550-560.
[21]
Evans, M.R.; James, C.D.; Loughran, O.; Nulton, T.J.; Wang, X.; Bristol, M.L.; Windle, B.; Morgan, I.M. An oral keratinocyte life cycle model identifies novel host genome regulation by human papillomavirus 16 relevant to HPV positive head and neck cancer. Oncotarget, 2017, 8(47), 81892-81909.
[22]
Iftner, T.; Haedicke-Jarboui, J.; Wu, S.Y.; Chiang, C.M. Involvement of Brd4 in different steps of the papillomavirus life cycle. Virus Res., 2017, 231, 76-82.
[24]
Xu, X-X.; Zhou, J.S.; Yuan, S.H.; Yu, H.; Lou, H.M. Distribution of HPV genotype in invasive cervical carcinoma and cervical intraepithelial neoplasia in Zhejiang province, southeast China: establishing the baseline for surveillance. Int. J. Environ. Res. Public Health, 2015, 12(9), 10794-10805.
[25]
Athinarayanan, S.; Srinath, M.; Kavitha, R. Detection and Classification
of Cervical Cancer in Pap Smear Images using EETCM,
EEETCM & CFE methods based Texture features and Various
Classification Techniques; IJSRSET, 2016.
[26]
Kessler, T.A. Cervical cancer: Prevention and early detection.Seminars in oncology nursing; Elsevier, 2017.
[27]
Bedoui, S.; Whitney, P.G.; Waithman, J.; Eidsmo, L.; Wakim, L.; Caminschi, I.; Allan, R.S.; Wojtasiak, M.; Shortman, K.; Carbone, F.R.; Brooks, A.G.; Heath, W.R. Cross-presentation of viral and self antigens by skin-derived CD103+ dendritic cells. Nat. Immunol., 2009, 10(5), 488-495.
[28]
Jenkins, D. Histopathology and cytopathology of cervical cancer. Dis. Markers, 2007, 23(4), 199-212.
[29]
Solomon, D.; Davey, D.; Kurman, R.; Moriarty, A.; O’Connor, D.; Prey, M.; Raab, S.; Sherman, M.; Wilbur, D.; Wright, T., Jr; Young, N. Forum Group Members Bethesda 2001 Workshop. The 2001 Bethesda System: terminology for reporting results of cervical cytology. JAMA, 2002, 287(16), 2114-2119.
[30]
Muñoz, N.; Bosch, F.X.; de Sanjosé, S.; Herrero, R.; Castellsagué, X.; Shah, K.V.; Snijders, P.J.; Meijer, C.J. International Agency for Research on Cancer Multicenter Cervical Cancer Study Group. Epidemiologic classification of human papillomavirus types associated with cervical cancer. N. Engl. J. Med., 2003, 348(6), 518-527.
[31]
Oliveira, L.B.; Haga, I.R.; Villa, L.L. Human papillomavirus (HPV) 16 E6 oncoprotein targets the Toll-like receptor pathway. J. Gen. Virol., 2018.
[32]
White, E.A.; Sowa, M.E.; Tan, M.J.; Jeudy, S.; Hayes, S.D.; Santha, S.; Münger, K.; Harper, J.W.; Howley, P.M. Systematic identification of interactions between host cell proteins and E7 oncoproteins from diverse human papillomaviruses. Proc. Natl. Acad. Sci. USA, 2012, 109(5), E260-E267.
[33]
Jiang, P.; Yue, Y. Human papillomavirus oncoproteins and apoptosis. (Review) Exp. Ther. Med., 2014, 7(1), 3-7.
[34]
White, E.A.; Münger, K.; Howley, P.M. High-risk human papillomavirus E7 proteins target PTPN14 for degradation. MBio, 2016, 7(5), e01530-e16.
[35]
Illiano, E.; Bissa, M.; Paolini, F.; Zanotto, C.; De Giuli Morghen, C.; Franconi, R.; Radaelli, A.; Venuti, A. Prime-boost therapeutic vaccination in mice with DNA/DNA or DNA/Fowlpox virus recombinants expressing the Human Papilloma Virus type 16 E6 and E7 mutated proteins fused to the coat protein of Potato virus X. Virus Res., 2016, 225, 82-90.
[36]
Wallace, N.A. High Risk Alpha Papillomavirus Oncogenes Impair
the Homologous Recombination Pathway; Journal of virology,
2017, p. JVI. 01084-17.
[37]
Harden, M.E.; Prasad, N.; Griffiths, A.; Munger, K. Modulation of microRNA-mRNA target pairs by human papillomavirus 16 oncoproteins. MBio, 2017, 8(1), e02170-e16.
[38]
Wang, X.; Wang, H.K.; Li, Y.; Hafner, M.; Banerjee, N.S.; Tang, S.; Briskin, D.; Meyers, C.; Chow, L.T.; Xie, X.; Tuschl, T.; Zheng, Z.M. microRNAs are biomarkers of oncogenic human papillomavirus infections. Proc. Natl. Acad. Sci. USA, 2014, 111(11), 4262-4267.
[39]
Mischo, A.; Ohlenschläger, O.; Hortschansky, P.; Ramachandran, R.; Görlach, M. Structural insights into a wildtype domain of the oncoprotein E6 and its interaction with a PDZ domain. PLoS One, 2013, 8(4), e62584.
[40]
Ristriani, T.; Nominé, Y.; Masson, M.; Weiss, E.; Travé, G. Specific recognition of four-way DNA junctions by the C-terminal zinc-binding domain of HPV oncoprotein E6. J. Mol. Biol., 2001, 305(4), 729-739.
[41]
Vande Pol, S.B.; Klingelhutz, A.J. Papillomavirus E6 oncoproteins. Virology, 2013, 445(1-2), 115-137.
[42]
Ganti, K.; Broniarczyk, J.; Manoubi, W.; Massimi, P.; Mittal, S.; Pim, D.; Szalmas, A.; Thatte, J.; Thomas, M.; Tomaić, V.; Banks, L. The human papillomavirus E6 PDZ binding motif: from life cycle to malignancy. Viruses, 2015, 7(7), 3530-3551.
[43]
Yeo-Teh, N.S.L.; Ito, Y.; Jha, S. High-risk human papillomaviral oncogenes E6 and E7 target key cellular pathways to achieve oncogenesis. Int. J. Mol. Sci., 2018, 19(6), 1706.
[44]
Lee, S.S.; Weiss, R.S.; Javier, R.T. Binding of human virus oncoproteins to hDlg/SAP97, a mammalian homolog of the Drosophila discs large tumor suppressor protein. Proc. Natl. Acad. Sci. USA, 1997, 94(13), 6670-6675.
[45]
Nakagawa, S.; Huibregtse, J.M. Human scribble (Vartul) is targeted for ubiquitin-mediated degradation by the high-risk papillomavirus E6 proteins and the E6AP ubiquitin-protein ligase. Mol. Cell. Biol., 2000, 20(21), 8244-8253.
[46]
Glaunsinger, B.A.; Lee, S.S.; Thomas, M.; Banks, L.; Javier, R. Interactions of the PDZ-protein MAGI-1 with adenovirus E4-ORF1 and high-risk papillomavirus E6 oncoproteins. Oncogene, 2000, 19(46), 5270-5280.
[47]
Massimi, P.; Shai, A.; Lambert, P.; Banks, L. HPV E6 degradation of p53 and PDZ containing substrates in an E6AP null background. Oncogene, 2008, 27(12), 1800-1804.
[48]
Martinez-Zapien, D.; Ruiz, F.X.; Poirson, J.; Mitschler, A.; Ramirez, J.; Forster, A.; Cousido-Siah, A.; Masson, M.; Vande Pol, S.; Podjarny, A.; Travé, G.; Zanier, K. Structure of the E6/E6AP/p53 complex required for HPV-mediated degradation of p53. Nature, 2016, 529(7587), 541-545.
[49]
Scheffner, M.; Werness, B.A.; Huibregtse, J.M.; Levine, A.J.; Howley, P.M. The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell, 1990, 63(6), 1129-1136.
[50]
Khoronenkova, S.V.; Dianov, G.L. The emerging role of Mule and ARF in the regulation of base excision repair. FEBS Lett., 2011, 585(18), 2831-2835.
[51]
Kumar, A.; Zhao, Y.; Meng, G.; Zeng, M.; Srinivasan, S.; Delmolino, L.M.; Gao, Q.; Dimri, G.; Weber, G.F.; Wazer, D.E.; Band, H.; Band, V. Human papillomavirus oncoprotein E6 inactivates the transcriptional coactivator human ADA3. Mol. Cell. Biol., 2002, 22(16), 5801-5812.
[52]
Nohata, N.; Hanazawa, T.; Enokida, H.; Seki, N. microRNA-1/133a and microRNA-206/133b clusters: dysregulation and functional roles in human cancers. Oncotarget, 2012, 3(1), 9-21.
[53]
Bommer, G.T.; Gerin, I.; Feng, Y.; Kaczorowski, A.J.; Kuick, R.; Love, R.E.; Zhai, Y.; Giordano, T.J.; Qin, Z.S.; Moore, B.B.; MacDougald, O.A.; Cho, K.R.; Fearon, E.R. p53-mediated activation of miRNA34 candidate tumor-suppressor genes. Curr. Biol., 2007, 17(15), 1298-1307.
[54]
Chang, T-C.; Wentzel, E.A.; Kent, O.A.; Ramachandran, K.; Mullendore, M.; Lee, K.H.; Feldmann, G.; Yamakuchi, M.; Ferlito, M.; Lowenstein, C.J.; Arking, D.E.; Beer, M.A.; Maitra, A.; Mendell, J.T. Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis. Mol. Cell, 2007, 26(5), 745-752.
[55]
Corney, D.C.; Flesken-Nikitin, A.; Godwin, A.K.; Wang, W.; Nikitin, A.Y. MicroRNA-34b and MicroRNA-34c are targets of p53 and cooperate in control of cell proliferation and adhesion-independent growth. Cancer Res., 2007, 67(18), 8433-8438.
[56]
Chen, A-H.; Qin, Y.E.; Tang, W.F.; Tao, J.; Song, H.M.; Zuo, M. MiR-34a and miR-206 act as novel prognostic and therapy biomarkers in cervical cancer. Cancer Cell Int., 2017, 17(1), 63.
[57]
Klingelhutz, A.J.; Foster, S.A.; McDougall, J.K. Telomerase activation
by the E6 gene product of human papillomavirus type 16.
nature 1996, 380(6569), 79.
[58]
Ganti, K.; Massimi, P.; Manzo-Merino, J.; Tomaić, V.; Pim, D.; Playford, M.P.; Lizano, M.; Roberts, S.; Kranjec, C.; Doorbar, J.; Banks, L. Interaction of the human papillomavirus E6 oncoprotein with sorting nexin 27 modulates endocytic cargo transport pathways. PLoS Pathog., 2016, 12(9), e1005854.
[59]
Kranjec, C.; Massimi, P.; Banks, L. Restoration of MAGI-1 expression in human papillomavirus-positive tumor cells induces cell growth arrest and apoptosis. J. Virol., 2014, 88(13), 7155-7169.
[60]
Mittal, S.; Banks, L. Molecular mechanisms underlying human papillomavirus E6 and E7 oncoprotein-induced cell transformation. Mutat. Res. Rev. Mutat. Res., 2017, 772, 23-35.
[61]
Hoppe-Seyler, K. The HPV E6/E7 oncogenes: Key factors for viral carcinogenesis and therapeutic targets. Trends Microbiol., 2017.
[62]
Sparrer, K.M.; Gack, M.U. Intracellular detection of viral nucleic acids. Curr. Opin. Microbiol., 2015, 26, 1-9.
[63]
Takeuchi, O.; Akira, S. Pattern recognition receptors and inflammation. Cell, 2010, 140(6), 805-820.
[64]
Chiang, C.; Pauli, E.K.; Biryukov, J.; Feister, K.F.; Meng, M.; White, E.A.; Münger, K.; Howley, P.M.; Meyers, C.; Gack, M.U. The human papillomavirus E6 oncoprotein targets USP15 and TRIM25 to suppress RIG-I-mediated innate immune signaling. J. Virol., 2018, 92(6), e01737-e17.
[65]
Chan, Y.K.; Gack, M.U. Viral evasion of intracellular DNA and RNA sensing. Nat. Rev. Microbiol., 2016, 14(6), 360-373.
[66]
Pauli, E-K.; Chan, Y.K.; Davis, M.E.; Gableske, S.; Wang, M.K.; Feister, K.F.; Gack, M.U. The ubiquitin-specific protease USP15 promotes RIG-I-mediated antiviral signaling by deubiquitylating TRIM25. Sci. Signal., 2014, 7(307), ra3-ra3.
[67]
Song, S.; Tan, J.; Miao, Y.; Zhang, Q. Crosstalk of ER stress-mediated autophagy and ER-phagy: Involvement of UPR and the core autophagy machinery. J. Cell. Physiol., 2018, 233(5), 3867-3874.
[68]
Kimmey, J.M.; Stallings, C.L. Bacterial pathogens versus autophagy: implications for therapeutic interventions. Trends Mol. Med., 2016, 22(12), 1060-1076.
[69]
Hamasaki, M.; Furuta, N.; Matsuda, A.; Nezu, A.; Yamamoto, A.; Fujita, N.; Oomori, H.; Noda, T.; Haraguchi, T.; Hiraoka, Y.; Amano, A.; Yoshimori, T. Autophagosomes form at ER-mitochondria contact sites. Nature, 2013, 495(7441), 389-393.
[70]
Ge, L.; Melville, D.; Zhang, M.; Schekman, R. The ER-Golgi intermediate compartment is a key membrane source for the LC3 lipidation step of autophagosome biogenesis. eLife, 2013, 2e0094,
[71]
Kim, Y.C.; Guan, K-L. mTOR: a pharmacologic target for autophagy regulation. J. Clin. Invest., 2015, 125(1), 25-32.
[72]
Stanley, R.E.; Ragusa, M.J.; Hurley, J.H. The beginning of the end: how scaffolds nucleate autophagosome biogenesis. Trends Cell Biol., 2014, 24(1), 73-81.
[73]
Choi, A.M.; Ryter, S.W.; Levine, B. Autophagy in human health and disease. N. Engl. J. Med., 2013, 368(7), 651-662.
[76]
Mattoscio, D.; Medda, A.; Chiocca, S. Human Papilloma Virus and Autophagy. Int. J. Mol. Sci., 2018, 19(6), 1775.
[77]
Bahrami, A.; Hasanzadeh, M.; Hassanian, S.M. ShahidSales, S.; Ghayour-Mobarhan, M.; Ferns, G.A.; Avan, A. The potential value of the PI3K/Akt/mTOR signaling pathway for assessing prognosis in cervical cancer and as a target for therapy. J. Cell. Biochem., 2017, 118(12), 4163-4169.
[78]
Surviladze, Z.; Dziduszko, A.; Ozbun, M.A. Essential roles for soluble virion-associated heparan sulfonated proteoglycans and growth factors in human papillomavirus infections. PLoS Pathog., 2012, 8(2), e1002519.
[79]
Surviladze, Z.; Sterk, R.T.; DeHaro, S.A.; Ozbun, M.A. Cellular entry of human papillomavirus type 16 involves activation of the phosphatidylinositol 3-kinase/Akt/mTOR pathway and inhibition of autophagy. J. Virol., 2013, 87(5), 2508-2517.
[80]
Papinski, D.; Kraft, C. Regulation of autophagy by signaling through the Atg1/ULK1 complex. J. Mol. Biol., 2016, 428(9 Pt A), 1725-1741.
[81]
Androphy, E.J.; Hubbert, N.L.; Schiller, J.T.; Lowy, D.R. Identification of the HPV-16 E6 protein from transformed mouse cells and human cervical carcinoma cell lines. EMBO J., 1987, 6(4), 989-992.
[82]
Banks, L.; Spence, P.; Androphy, E.; Hubbert, N.; Matlashewski, G.; Murray, A.; Crawford, L. Identification of human papillomavirus type 18 E6 polypeptide in cells derived from human cervical carcinomas. J. Gen. Virol., 1987, 68(Pt 5), 1351-1359.
[83]
Goodwin, E.C.; DiMaio, D. Repression of human papillomavirus oncogenes in HeLa cervical carcinoma cells causes the orderly reactivation of dormant tumor suppressor pathways. Proc. Natl. Acad. Sci. USA, 2000, 97(23), 12513-12518.
[84]
Scheffner, M.; Huibregtse, J.M.; Vierstra, R.D.; Howley, P.M. The HPV-16 E6 and E6-AP complex functions as a ubiquitin-protein ligase in the ubiquitination of p53. Cell, 1993, 75(3), 495-505.
[85]
Itahana, Y.; Itahana, K. Emerging roles of p53 family members in glucose metabolism. Int. J. Mol. Sci., 2018, 19(3), 776.
[86]
Matoba, S.; Kang, J.G.; Patino, W.D.; Wragg, A.; Boehm, M.; Gavrilova, O.; Hurley, P.J.; Bunz, F.; Hwang, P.M. p53 regulates mitochondrial respiration. Science, 2006, 312(5780), 1650-1653.
[87]
Veldman, T.; Liu, X.; Yuan, H.; Schlegel, R. Human papillomavirus E6 and Myc proteins associate in vivo and bind to and cooperatively activate the telomerase reverse transcriptase promoter. Proc. Natl. Acad. Sci. USA, 2003, 100(14), 8211-8216.
[89]
Rodolico, V.; Arancio, W.; Amato, M.C.; Aragona, F.; Cappello, F.; Di Fede, O.; Pannone, G.; Campisi, G. Hypoxia inducible factor-1 alpha expression is increased in infected positive HPV16 DNA oral squamous cell carcinoma and positively associated with HPV16 E7 oncoprotein. Infect. Agent. Cancer, 2011, 6(1), 18.
[90]
Masoud, G.N.; Li, W. HIF-1α pathway: role, regulation and intervention for cancer therapy. Acta Pharm. Sin. B, 2015, 5(5), 378-389.
[91]
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.
[92]
Stambolsky, P.; Weisz, L.; Shats, I.; Klein, Y.; Goldfinger, N.; Oren, M.; Rotter, V. Regulation of AIF expression by p53. Cell Death Differ., 2006, 13(12), 2140-2149.
[93]
Liu, G.; Chen, X. The ferredoxin reductase gene is regulated by the p53 family and sensitizes cells to oxidative stress-induced apoptosis. Oncogene, 2002, 21(47), 7195-7204.
[94]
Suzuki, S.; Tanaka, T.; Poyurovsky, M.V.; Nagano, H.; Mayama, T.; Ohkubo, S.; Lokshin, M.; Hosokawa, H.; Nakayama, T.; Suzuki, Y.; Sugano, S.; Sato, E.; Nagao, T.; Yokote, K.; Tatsuno, I.; Prives, C. Phosphate-activated glutaminase (GLS2), a p53-inducible regulator of glutamine metabolism and reactive oxygen species. Proc. Natl. Acad. Sci. USA, 2010, 107(16), 7461-7466.
[95]
Liu, Y.; Murray-Stewart, T.; Casero, R.A., Jr; Kagiampakis, I.; Jin, L.; Zhang, J.; Wang, H.; Che, Q.; Tong, H.; Ke, J.; Jiang, F.; Wang, F.; Wan, X. Targeting hexokinase 2 inhibition promotes radiosensitization in HPV16 E7-induced cervical cancer and suppresses tumor growth. Int. J. Oncol., 2017, 50(6), 2011-2023.
[96]
Kim, S.M.; Yun, M.R.; Hong, Y.K.; Solca, F.; Kim, J.H.; Kim, H.J.; Cho, B.C. Glycolysis inhibition sensitizes non-small cell lung cancer with T790M mutation to irreversible EGFR inhibitors via translational suppression of Mcl-1 by AMPK activation. Mol. Cancer Ther., 2013, 12(10), 2145-2156.
[97]
Komurov, K.; Tseng, J.T.; Muller, M.; Seviour, E.G.; Moss, T.J.; Yang, L.; Nagrath, D.; Ram, P.T. The glucose-deprivation network counteracts lapatinib-induced toxicity in resistant ErbB2-positive breast cancer cells. Mol. Syst. Biol., 2012, 8(1), 596.
[98]
Calin, G.A.; Croce, C.M. MicroRNA signatures in human cancers. Nat. Rev. Cancer, 2006, 6(11), 857-866.
[99]
Esquela-Kerscher, A.; Slack, F.J. Oncomirs - microRNAs with a role in cancer. Nat. Rev. Cancer, 2006, 6(4), 259-269.
[100]
Garzon, R.; Fabbri, M.; Cimmino, A.; Calin, G.A.; Croce, C.M. MicroRNA expression and function in cancer. Trends Mol. Med., 2006, 12(12), 580-587.
[101]
Zhou, R.; Hu, G.; Gong, A.Y.; Chen, X.M. Binding of NF-kappaB p65 subunit to the promoter elements is involved in LPS-induced transactivation of miRNA genes in human biliary epithelial cells. Nucleic Acids Res., 2010, 38(10), 3222-3232.
[102]
Gao, P.; Tchernyshyov, I.; Chang, T.C.; Lee, Y.S.; Kita, K.; Ochi, T.; Zeller, K.I.; De Marzo, A.M.; Van Eyk, J.E.; Mendell, J.T.; Dang, C.V. c-Myc suppression of miR-23a/b enhances mitochondrial glutaminase expression and glutamine metabolism. Nature, 2009, 458(7239), 762-765.
[103]
Maulik, G.; Shrikhande, A.; Kijima, T.; Ma, P.C.; Morrison, P.T.; Salgia, R. Role of the hepatocyte growth factor receptor, c-Met, in oncogenesis and potential for therapeutic inhibition. Cytokine Growth Factor Rev., 2002, 13(1), 41-59.
[104]
Baykal, C.; Ayhan, A.; Al, A.; Yüce, K.; Ayhan, A. Overexpression of the c-Met/HGF receptor and its prognostic significance in uterine cervix carcinomas. Gynecol. Oncol., 2003, 88(2), 123-129.
[105]
Tsai, H-W.; Chow, N.H.; Lin, C.P.; Chan, S.H.; Chou, C.Y.; Ho, C.L. The significance of prohibitin and c-Met/hepatocyte growth factor receptor in the progression of cervical adenocarcinoma. Hum. Pathol., 2006, 37(2), 198-204.
[106]
Yeung, C.L.A.; Tsang, T.Y.; Yau, P.L.; Kwok, T.T. Human papillomavirus type 16 E6 suppresses microRNA-23b expression in human cervical cancer cells through DNA methylation of the host gene C9orf3. Oncotarget, 2017, 8(7), 12158-12173.
[107]
Au Yeung, C.L.; Tsang, T.Y.; Yau, P.L.; Kwok, T.T. Human papillomavirus type 16 E6 induces cervical cancer cell migration through the p53/microRNA-23b/urokinase-type plasminogen activator pathway. Oncogene, 2011, 30(21), 2401-2410.
[109]
Zhang, W.; Chen, H.; Chen, Y.; Liu, J.; Wang, X.; Yu, X.; Chen, J.J.; Zhao, W. Cancerous inhibitor of protein phosphatase 2A contributes to human papillomavirus oncoprotein E7-induced cell proliferation via E2F1. Oncotarget, 2015, 6(7), 5253-5262.
[110]
McKinney, C.C.; Kim, M.J.; Chen, D.; McBride, A.A. Brd4 Activates Early Viral Transcription upon Human Papillomavirus 18 Infection of Primary Keratinocytes. MBio, 2016, 7(6), e01644-e16.
[111]
Zhou, F.; Chen, J.; Zhao, K-N. Human papillomavirus 16-encoded E7 protein inhibits IFN-γ-mediated MHC class I antigen presentation and CTL-induced lysis by blocking IRF-1 expression in mouse keratinocytes. J. Gen. Virol., 2013, 94(Pt 11), 2504-2514.
[112]
Kalfert, D.; Ludvikova, M.; Topolcan, O.; Celakovsky, P.; Kucera, R.; Windrichova, J.; Ludvik, J.; Skalova, K.; Kulda, V.; Pesta, M.; Plzak, J. Serum Levels of IGF-1 and IGFBP-3 in Relation to Clinical and Pathobiological Aspects of Head and Neck Squamous Cell Carcinomas. Anticancer Res., 2017, 37(6), 3281-3286.
[113]
Doorbar, J.; Egawa, N.; Griffin, H.; Kranjec, C.; Murakami, I. Human papillomavirus molecular biology and disease association. Rev. Med. Virol., 2015, 25(S1)(Suppl. 1), 2-23.
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