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Current Cancer Drug Targets

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ISSN (Print): 1568-0096
ISSN (Online): 1873-5576

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Review Article

Effect of HPV Oncoprotein on Carbohydrate and Lipid Metabolism in Tumor Cells

Author(s): Biqing Chen, Yichao Wang, Yishi Wu and Tianmin Xu*

Volume 24, Issue 10, 2024

Published on: 26 January, 2024

Page: [987 - 1004] Pages: 18

DOI: 10.2174/0115680096266981231215111109

Price: $65

Abstract

High-risk HPV infection accounts for 99.7% of cervical cancer, over 90% of anal cancer, 50% of head and neck cancers, 40% of vulvar cancer, and some cases of vaginal and penile cancer, contributing to approximately 5% of cancers worldwide. The development of cancer is a complex, multi-step process characterized by dysregulation of signaling pathways and alterations in metabolic pathways. Extensive research has demonstrated that metabolic reprogramming plays a key role in the progression of various cancers, such as cervical, head and neck, bladder, and prostate cancers, providing the material and energy foundation for rapid proliferation and migration of cancer cells. Metabolic reprogramming of tumor cells allows for the rapid generation of ATP, aiding in meeting the high energy demands of HPV-related cancer cell proliferation. The interaction between Human Papillomavirus (HPV) and its associated cancers has become a recent focus of investigation. The impact of HPV on cellular metabolism has emerged as an emerging research topic. A significant body of research has shown that HPV influences relevant metabolic signaling pathways, leading to cellular metabolic alterations. Exploring the underlying mechanisms may facilitate the discovery of biomarkers for diagnosis and treatment of HPV-associated diseases. In this review, we introduced the molecular structure of HPV and its replication process, discussed the diseases associated with HPV infection, described the energy metabolism of normal cells, highlighted the metabolic features of tumor cells, and provided an overview of recent advances in potential therapeutic targets that act on cellular metabolism. We discussed the potential mechanisms underlying these changes. This article aims to elucidate the role of Human Papillomavirus (HPV) in reshaping cellular metabolism and the application of metabolic changes in the research of related diseases. Targeting cancer metabolism may serve as an effective strategy to support traditional cancer treatments, as metabolic reprogramming is crucial for malignant transformation in cancer.

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[1]
Warburg, O. On the origin of cancer cells. Science, 1956, 123(3191), 309-314.
[http://dx.doi.org/10.1126/science.123.3191.309] [PMID: 13298683]
[2]
Hanahan, D.; Weinberg, R.A. Hallmarks of cancer: The next generation. Cell, 2011, 144(5), 646-674.
[http://dx.doi.org/10.1016/j.cell.2011.02.013] [PMID: 21376230]
[3]
Aydin, I.; Weber, S.; Snijder, B.; Samperio, V.P.; Kühbacher, A.; Becker, M.; Day, P.M.; Schiller, J.T.; Kann, M.; Pelkmans, L.; Helenius, A.; Schelhaas, M. Large scale RNAi reveals the requirement of nuclear envelope breakdown for nuclear import of human papillomaviruses. PLoS Pathog., 2014, 10(5), e1004162.
[http://dx.doi.org/10.1371/journal.ppat.1004162] [PMID: 24874089]
[4]
Chen, C.C.; Li, B.; Millman, S.E.; Chen, C.; Li, X.; Morris, J.P., IV; Mayle, A.; Ho, Y.J.; Loizou, E.; Liu, H.; Qin, W.; Shah, H.; Violante, S.; Cross, J.R.; Lowe, S.W.; Zhang, L. Vitamin B6 addiction in acute myeloid leukemia. Cancer Cell, 2020, 37(1), 71-84.e7.
[http://dx.doi.org/10.1016/j.ccell.2019.12.002] [PMID: 31935373]
[5]
Sonnenschein, C.; Soto, A.M. The aging of the 2000 and 2011 Hallmarks of Cancer reviews: A critique. J. Biosci., 2013, 38(3), 651-663.
[http://dx.doi.org/10.1007/s12038-013-9335-6] [PMID: 23938395]
[6]
Pavlova, N.N.; Thompson, C.B. The emerging hallmarks of cancer metabolism. Cell Metab., 2016, 23(1), 27-47.
[http://dx.doi.org/10.1016/j.cmet.2015.12.006] [PMID: 26771115]
[7]
Lévy, P.; Bartosch, B. Metabolic reprogramming: A hallmark of viral oncogenesis. Oncogene, 2016, 35(32), 4155-4164.
[http://dx.doi.org/10.1038/onc.2015.479] [PMID: 26686092]
[8]
Jones, R.G.; Thompson, C.B. Tumor suppressors and cell metabolism: A recipe for cancer growth. Genes Dev., 2009, 23(5), 537-548.
[http://dx.doi.org/10.1101/gad.1756509] [PMID: 19270154]
[9]
DeBerardinis, R.J.; Lum, J.J.; Hatzivassiliou, G.; Thompson, C.B. The biology of cancer: Metabolic reprogramming fuels cell growth and proliferation. Cell Metab., 2008, 7(1), 11-20.
[http://dx.doi.org/10.1016/j.cmet.2007.10.002] [PMID: 18177721]
[10]
Xu, Y.; Miriyala, S.; Fang, F.; Bakthavatchalu, V.; Noel, T.; Schell, D.M.; Wang, C.; St Clair, W.H.; St Clair, D.K. Manganese superoxide dismutase deficiency triggers mitochondrial uncoupling and the Warburg effect. Oncogene, 2015, 34(32), 4229-4237.
[http://dx.doi.org/10.1038/onc.2014.355] [PMID: 25362851]
[11]
Doherty, J.R.; Cleveland, J.L. Targeting lactate metabolism for cancer therapeutics. J. Clin. Invest., 2013, 123(9), 3685-3692.
[http://dx.doi.org/10.1172/JCI69741] [PMID: 23999443]
[12]
Xia, C.; Li, S.; Long, T.; Chen, Z.; Chan, P.K.S.; Boon, S.S. Current updates on cancer-causing types of human papillomaviruses (HPVs) in East, Southeast, and South Asia. Cancers, 2021, 13(11), 2691.
[http://dx.doi.org/10.3390/cancers13112691] [PMID: 34070706]
[13]
Egawa, N.; Egawa, K.; Griffin, H.; Doorbar, J. Human papillomaviruses; Epithelial tropisms, and the development of neoplasia. Viruses, 2015, 7(7), 3863-3890.
[http://dx.doi.org/10.3390/v7072802] [PMID: 26193301]
[14]
Dreer, M.; Blondzik, S.; Straub, E.; Iftner, T.; Stubenrauch, F. Contribution of HDAC3 to transcriptional repression by the human papillomavirus 31 E8^E2 protein. J. Gen. Virol., 2020, 101(7), 751-759.
[http://dx.doi.org/10.1099/jgv.0.001438] [PMID: 32421493]
[15]
Frattini, M.G.; Lim, H.B.; Laimins, L.A. In vitro synthesis of oncogenic human papillomaviruses requires episomal genomes for differentiation-dependent late expression. Proc. Natl. Acad. Sci., 1996, 93(7), 3062-3067.
[http://dx.doi.org/10.1073/pnas.93.7.3062] [PMID: 8610168]
[16]
Park, R.B.; Androphy, E.J. Genetic analysis of high-risk e6 in episomal maintenance of human papillomavirus genomes in primary human keratinocytes. J. Virol., 2002, 76(22), 11359-11364.
[http://dx.doi.org/10.1128/JVI.76.22.11359-11364.2002] [PMID: 12388696]
[17]
Doorbar, J. The E4 protein; structure, function and patterns of expression. Virology, 2013, 445(1-2), 80-98.
[http://dx.doi.org/10.1016/j.virol.2013.07.008] [PMID: 24016539]
[18]
Suprynowicz, F.A.; Krawczyk, E.; Hebert, J.D.; Sudarshan, S.R.; Simic, V.; Kamonjoh, C.M.; Schlegel, R. The human papillomavirus type 16 E5 oncoprotein inhibits epidermal growth factor trafficking independently of endosome acidification. J. Virol., 2010, 84(20), 10619-10629.
[http://dx.doi.org/10.1128/JVI.00831-10] [PMID: 20686024]
[19]
Venuti, A.; Paolini, F.; Nasir, L.; Corteggio, A.; Roperto, S.; Campo, M.S.; Borzacchiello, G. Papillomavirus E5: The smallest oncoprotein with many functions. Mol. Cancer, 2011, 10(1), 140.
[http://dx.doi.org/10.1186/1476-4598-10-140] [PMID: 22078316]
[20]
Yeo-Teh, N.; 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.
[http://dx.doi.org/10.3390/ijms19061706] [PMID: 29890655]
[21]
Buck, C.B.; Cheng, N.; Thompson, C.D.; Lowy, D.R.; Steven, A.C.; Schiller, J.T.; Trus, B.L. Arrangement of L2 within the papillomavirus capsid. J. Virol., 2008, 82(11), 5190-5197.
[http://dx.doi.org/10.1128/JVI.02726-07] [PMID: 18367526]
[22]
Yan, H.; Foo, S.S.; Chen, W.; Yoo, J.S.; Shin, W.J.; Wu, C.; Jung, J.U. Efficient inhibition of human papillomavirus infection by L2 minor capsid-derived lipopeptide. MBio, 2019, 10(4), e01834-19.
[http://dx.doi.org/10.1128/mBio.01834-19] [PMID: 31387913]
[23]
Shafti-Keramat, S.; Handisurya, A.; Kriehuber, E.; Meneguzzi, G.; Slupetzky, K.; Kirnbauer, R. Different heparan sulfate proteoglycans serve as cellular receptors for human papillomaviruses. J. Virol., 2003, 77(24), 13125-13135.
[http://dx.doi.org/10.1128/JVI.77.24.13125-13135.2003] [PMID: 14645569]
[24]
Stanley, M.A. Epithelial cell responses to infection with human papillomavirus. Clin. Microbiol. Rev., 2012, 25(2), 215-222.
[http://dx.doi.org/10.1128/CMR.05028-11] [PMID: 22491770]
[25]
Spoden, G.; Freitag, K.; Husmann, M.; Boller, K.; Sapp, M.; Lambert, C.; Florin, L. 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]
[26]
Mac, M.; Moody, C.A. Epigenetic regulation of the human papillomavirus life cycle. Pathogens, 2020, 9(6), 483.
[http://dx.doi.org/10.3390/pathogens9060483] [PMID: 32570816]
[27]
McLaughlin-Drubin, M.E.; Christensen, N.D.; Meyers, C. Propagation, infection, and neutralization of authentic HPV16 virus. Virology, 2004, 322(2), 213-219.
[http://dx.doi.org/10.1016/j.virol.2004.02.011] [PMID: 15110519]
[28]
Coupe, V.M.; González-Barreiro, L.; Gutiérrez-Berzal, J.; Melián-Bóveda, A.L.; López-Rodríguez, O.; Alba-Domínguez, J.; Alba-Losada, J. Transcriptional analysis of human papillomavirus type 16 in histological sections of cervical dysplasia by in situ hybridisation. J. Clin. Pathol., 2012, 65(2), 164-170.
[http://dx.doi.org/10.1136/jclinpath-2011-200330] [PMID: 22075186]
[29]
Rodríguez, A.C.; Schiffman, M.; Herrero, R.; Wacholder, S.; Hildesheim, A.; Castle, P.E.; Solomon, D.; Burk, R. Rapid clearance of human papillomavirus and implications for clinical focus on persistent infections. J. Natl. Cancer Inst., 2008, 100(7), 513-517.
[http://dx.doi.org/10.1093/jnci/djn044] [PMID: 18364507]
[30]
Vinokurova, S.; Wentzensen, N.; Kraus, I.; Klaes, R.; Driesch, C.; Melsheimer, P.; Kisseljov, F.; Dürst, M.; Schneider, A.; von Knebel, D.M. Type-dependent integration frequency of human papillomavirus genomes in cervical lesions. Cancer Res., 2008, 68(1), 307-313.
[http://dx.doi.org/10.1158/0008-5472.CAN-07-2754] [PMID: 18172324]
[31]
Li, W.; Tian, S.; Wang, P.; Zang, Y.; Chen, X.; Yao, Y.; Li, W. The characteristics of HPV integration in cervical intraepithelial cells. J. Cancer, 2019, 10(12), 2783-2787.
[http://dx.doi.org/10.7150/jca.31450] [PMID: 31258786]
[32]
Vojtechova, Z.; Sabol, I.; Salakova, M.; Turek, L.; Grega, M.; Smahelova, J.; Vencalek, O.; Lukesova, E.; Klozar, J.; Tachezy, R. Analysis of the integration of human papillomaviruses in head and neck tumours in relation to patients’ prognosis. Int. J. Cancer, 2016, 138(2), 386-395.
[http://dx.doi.org/10.1002/ijc.29712] [PMID: 26239888]
[33]
McBride, A.A.; Warburton, A.; 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]
[34]
Doorbar, J. Molecular biology of human papillomavirus infection and cervical cancer. Clin. Sci., 2006, 110(5), 525-541.
[http://dx.doi.org/10.1042/CS20050369] [PMID: 16597322]
[35]
Hiller, T.; Poppelreuther, S.; Stubenrauch, F.; Iftner, T. Comparative analysis of 19 genital human papillomavirus types with regard to p53 degradation, immortalization, phylogeny, and epidemiologic risk classification. Cancer Epidemiol. Biomarkers Prev., 2006, 15(7), 1262-1267.
[http://dx.doi.org/10.1158/1055-9965.EPI-05-0778] [PMID: 16835321]
[36]
Zhang, B.; Chen, W.; Roman, A. The E7 proteins of low- and high-risk human papillomaviruses share the ability to target the pRB family member p130 for degradation. Proc. Natl. Acad. Sci., 2006, 103(2), 437-442.
[http://dx.doi.org/10.1073/pnas.0510012103] [PMID: 16381817]
[37]
Gray, E.; Pett, M.R.; Ward, D.; Winder, D.M.; Stanley, M.A.; Roberts, I.; Scarpini, C.G.; Coleman, N. In vitro progression of human papillomavirus 16 episome-associated cervical neoplasia displays fundamental similarities to integrant-associated carcinogenesis. Cancer Res., 2010, 70(10), 4081-4091.
[http://dx.doi.org/10.1158/0008-5472.CAN-09-3335] [PMID: 20442284]
[38]
de Villiers, E.M. Cross-roads in the classification of papillomaviruses. Virology, 2013, 445(1-2), 2-10.
[http://dx.doi.org/10.1016/j.virol.2013.04.023] [PMID: 23683837]
[39]
Screening for cervical cancer. CA Cancer J. Clin., 2020, 70(5), 347-348.
[http://dx.doi.org/10.3322/caac.21629] [PMID: 33460047]
[40]
Horvath, J.D.C.; Kops, N.L.; Caierão, J.; Bessel, M.; Hohenberger, G.; Wendland, E.M. Human papillomavirus knowledge, beliefs, and behaviors: A questionnaire adaptation. Eur. J. Obstet. Gynecol. Reprod. Biol., 2018, 230, 103-108.
[http://dx.doi.org/10.1016/j.ejogrb.2018.09.023] [PMID: 30248535]
[41]
Cubie, H.A. Diseases associated with human papillomavirus infection. Virology, 2013, 445(1-2), 21-34.
[http://dx.doi.org/10.1016/j.virol.2013.06.007] [PMID: 23932731]
[42]
Sniadecki, M.; Swierzko, A.; Dabkowski, M.; Orlowska-Volk, M.; Wycinka, E.; Klasa-Mazurkiewicz, D.; Milewska, A.; Poniewierza, P.; Liro, M.; Wydra, D. New therapeutic approaches in the treatment of node-positive cervical cancer patients based on molecular targets: A systematic review. Ginekol. Pol., 2019, 90(6), 336-345.
[http://dx.doi.org/10.5603/GP.2019.0062] [PMID: 31276186]
[43]
Torous, V.F.; Oliva, E. On the new (version 9) American Joint Committee on Cancer tumor, node, metastasis staging for cervical cancer—A commentary. Cancer Cytopathol., 2021, 129(8), 581-582.
[http://dx.doi.org/10.1002/cncy.22486] [PMID: 34161669]
[44]
Chatterjee, K.; Mukherjee, S.; Vanmanen, J.; Banerjee, P.; Fata, J.E. Dietary polyphenols, resveratrol and pterostilbene exhibit antitumor activity on an HPV E6-positive cervical cancer model: An in vitro and in vivo analysis. Front. Oncol., 2019, 9, 352.
[http://dx.doi.org/10.3389/fonc.2019.00352] [PMID: 31143704]
[45]
Hong, C.M.; Park, S.H.; Chong, G.O.; Lee, Y.H.; Jeong, J.H.; Lee, S.W.; Lee, J.; Ahn, B.C.; Jeong, S.Y. Enhancing prognosis prediction using pre-treatment nodal SUVmax and HPV status in cervical squamous cell carcinoma. Cancer Imaging, 2019, 19(1), 43.
[http://dx.doi.org/10.1186/s40644-019-0226-4] [PMID: 31234933]
[46]
Muñoz, N.; Bosch, F.X.; de Sanjosé, S.; Herrero, R.; Castellsagué, X.; Shah, K.V.; Snijders, P.J.F.; Meijer, C.J.L.M. Epidemiologic classification of human papillomavirus types associated with cervical cancer. N. Engl. J. Med., 2003, 348(6), 518-527.
[http://dx.doi.org/10.1056/NEJMoa021641] [PMID: 12571259]
[47]
de Sanjosé, S.; Brotons, M.; Pavón, M.A. The natural history of human papillomavirus infection. Best Pract. Res. Clin. Obstet. Gynaecol., 2018, 47, 2-13.
[http://dx.doi.org/10.1016/j.bpobgyn.2017.08.015] [PMID: 28964706]
[48]
Monsonego, J.; Cox, J.T.; Behrens, C.; Sandri, M.; Franco, E.L.; Yap, P.S.; Huh, W. Prevalence of high-risk human papilloma virus genotypes and associated risk of cervical precancerous lesions in a large U.S. screening population: Data from the ATHENA trial. Gynecol. Oncol., 2015, 137(1), 47-54.
[http://dx.doi.org/10.1016/j.ygyno.2015.01.551] [PMID: 25667973]
[49]
Parkin, D.M.; Bray, F. Chapter 2: The burden of HPV-related cancers. Vaccine, 2006, 24(S3), S11-S25, 11-25.
[http://dx.doi.org/10.1016/j.vaccine.2006.05.111] [PMID: 16949997]
[50]
Ndiaye, C.; Mena, M.; Alemany, L.; Arbyn, M.; Castellsagué, X.; Laporte, L.; Bosch, F.X.; de Sanjosé, S.; Trottier, H. HPV DNA, E6/E7 mRNA, and p16INK4a detection in head and neck cancers: A systematic review and meta-analysis. Lancet Oncol., 2014, 15(12), 1319-1331.
[http://dx.doi.org/10.1016/S1470-2045(14)70471-1] [PMID: 25439690]
[51]
Bouwes Bavinck, J.N.; Feltkamp, M.C.W.; Green, A.C.; Fiocco, M.; Euvrard, S.; Harwood, C.A.; Nasir, S.; Thomson, J.; Proby, C.M.; Naldi, L.; Diphoorn, J.C.D.; Venturuzzo, A.; Tessari, G.; Nindl, I.; Sampogna, F.; Abeni, D.; Neale, R.E.; Goeman, J.J.; Quint, K.D.; Halk, A.B.; Sneek, C.; Genders, R.E.; de Koning, M.N.C.; Quint, W.G.V.; Wieland, U.; Weissenborn, S.; Waterboer, T.; Pawlita, M.; Pfister, H. Human papillomavirus and posttransplantation cutaneous squamous cell carcinoma: A multicenter, prospective cohort study. Am. J. Transplant., 2018, 18(5), 1220-1230.
[http://dx.doi.org/10.1111/ajt.14537] [PMID: 29024374]
[52]
Hasche, D.; Vinzón, S.E.; Rösl, F. Cutaneous papillomaviruses and non-melanoma skin cancer: Causal agents or innocent bystanders? Front. Microbiol., 2018, 9, 874.
[http://dx.doi.org/10.3389/fmicb.2018.00874] [PMID: 29770129]
[53]
Rollison, D.E.; Viarisio, D.; Amorrortu, R.P.; Gheit, T.; Tommasino, M.; Sullivan, C.S. An emerging issue in oncogenic virology: The role of beta human papillomavirus types in the development of cutaneous squamous cell carcinoma. J. Virol., 2019, 93(7), e01003-18.
[http://dx.doi.org/10.1128/JVI.01003-18] [PMID: 30700603]
[54]
Handisurya, A.; Schellenbacher, C.; Kirnbauer, R. Diseases caused by human papillomaviruses (HPV). J. Dtsch. Dermatol. Ges., 2009, 7(5), 453-466.
[PMID: 19302229]
[55]
Wangu, Z.; Hsu, K.K. Impact of HPV vaccination on anogenital warts and respiratory papillomatosis. Hum. Vaccin. Immunother., 2016, 12(6), 1357-1362.
[http://dx.doi.org/10.1080/21645515.2016.1172754] [PMID: 27217191]
[56]
Sarbu, M.I.; Sarbu, I.F.; Tampa, M.; Benea, V.; Nicolae, I.; Matei, C.; Poteca, T.; Georgescu, S.R. Buschke-Löwenstein tumor of the vulva in a patient with a history of squamous cell carcinoma of the cervix. BMC Infect. Dis., 2014, 14(S7), P11.
[http://dx.doi.org/10.1186/1471-2334-14-S7-P11]
[57]
Miranda, P.M.; Silva, N.N.T.; Pitol, B.C.V.; Silva, I.D.C.G.; Lima-Filho, J.L.; Carvalho, R.F.; Stocco, R.C.; Beçak, W.; Lima, A.A. Persistence or clearance of human papillomavirus infections in women in Ouro Preto, Brazil. BioMed Res. Int., 2013, 2013, 1-6.
[http://dx.doi.org/10.1155/2013/578276] [PMID: 24298551]
[58]
Maehama, T.; Patzelt, A.; Lengert, M.; Hutter, K.J.; Kanazawa, K.; Zur Hausen, H.; Rösl, F. Selective down-regulation of human papillomavirus transcription by 2-deoxyglucose. Int. J. Cancer, 1998, 76(5), 639-646.
[http://dx.doi.org/10.1002/(SICI)1097-0215(19980529)76:5<639::AID-IJC5>3.0.CO;2-R] [PMID: 9610719]
[59]
Ward, P.S.; Thompson, C.B. Metabolic reprogramming: A cancer hallmark even warburg did not anticipate. Cancer Cell, 2012, 21(3), 297-308.
[http://dx.doi.org/10.1016/j.ccr.2012.02.014] [PMID: 22439925]
[60]
Lu, J. The Warburg metabolism fuels tumor metastasis. Cancer Metastasis Rev., 2019, 38(1-2), 157-164.
[http://dx.doi.org/10.1007/s10555-019-09794-5] [PMID: 30997670]
[61]
Vander Heiden, M.G.; Cantley, L.C.; Thompson, C.B. Understanding the warburg effect: The metabolic requirements of cell proliferation. Science, 2009, 324(5930), 1029-1033.
[http://dx.doi.org/10.1126/science.1160809] [PMID: 19460998]
[62]
Schurr, A.; West, C.A.; Rigor, B.M. Lactate-supported synaptic function in the rat hippocampal slice preparation. Science, 1988, 240(4857), 1326-1328.
[http://dx.doi.org/10.1126/science.3375817] [PMID: 3375817]
[63]
Koppenol, W.H.; Bounds, P.L.; Dang, C.V. Otto Warburg’s contributions to current concepts of cancer metabolism. Nat. Rev. Cancer, 2011, 11(5), 325-337.
[http://dx.doi.org/10.1038/nrc3038] [PMID: 21508971]
[64]
Metallo, C.M.; Gameiro, P.A.; Bell, E.L.; Mattaini, K.R.; Yang, J.; Hiller, K.; Jewell, C.M.; Johnson, Z.R.; Irvine, D.J.; Guarente, L.; Kelleher, J.K.; Vander Heiden, M.G.; Iliopoulos, O.; Stephanopoulos, G. Reductive glutamine metabolism by IDH1 mediates lipogenesis under hypoxia. Nature, 2012, 481(7381), 380-384.
[http://dx.doi.org/10.1038/nature10602] [PMID: 22101433]
[65]
Liberti, M.V.; Locasale, J.W. The warburg effect: How does it benefit cancer cells? Trends Biochem. Sci., 2016, 41(3), 211-218.
[http://dx.doi.org/10.1016/j.tibs.2015.12.001] [PMID: 26778478]
[66]
Jones, W.; Bianchi, K. Aerobic glycolysis: Beyond proliferation. Front. Immunol., 2015, 6, 227.
[http://dx.doi.org/10.3389/fimmu.2015.00227] [PMID: 26029212]
[67]
Woods, M.W.; duBuy, H.G. Cytoplasmic diseases and cancer. Science, 1945, 102(2658), 591-593.
[http://dx.doi.org/10.1126/science.102.2658.591]
[68]
Moreno-Sánchez, R.; Rodríguez-Enríquez, S.; Marín-Hernández, A.; Saavedra, E. Energy metabolism in tumor cells. FEBS J., 2007, 274(6), 1393-1418.
[http://dx.doi.org/10.1111/j.1742-4658.2007.05686.x] [PMID: 17302740]
[69]
Fantin, V.R.; St-Pierre, J.; Leder, P. Attenuation of LDH-A expression uncovers a link between glycolysis, mitochondrial physiology, and tumor maintenance. Cancer Cell, 2006, 9(6), 425-434.
[http://dx.doi.org/10.1016/j.ccr.2006.04.023] [PMID: 16766262]
[70]
Gottschalk, S.; Anderson, N.; Hainz, C.; Eckhardt, S.G.; Serkova, N.J. Imatinib (STI571)-mediated changes in glucose metabolism in human leukemia BCR-ABL-positive cells. Clin. Cancer Res., 2004, 10(19), 6661-6668.
[http://dx.doi.org/10.1158/1078-0432.CCR-04-0039] [PMID: 15475456]
[71]
Zhan, C.; Yan, L.; Wang, L.; Ma, J.; Jiang, W.; Zhang, Y.; Shi, Y.; Wang, Q. Isoform switch of pyruvate kinase M1 indeed occurs but not to pyruvate kinase M2 in human tumorigenesis. PLoS One, 2015, 10(3), e0118663.
[http://dx.doi.org/10.1371/journal.pone.0118663] [PMID: 25738776]
[72]
Ge, T.; Yang, J.; Zhou, S.; Wang, Y.; Li, Y.; Tong, X. The role of the pentose phosphate pathway in diabetes and cancer. Front. Endocrinol., 2020, 11, 365.
[http://dx.doi.org/10.3389/fendo.2020.00365] [PMID: 32582032]
[73]
Burns, J.; Manda, G. Metabolic pathways of the warburg effect in health and disease: Perspectives of choice, chain or chance. Int. J. Mol. Sci., 2017, 18(12), 2755.
[http://dx.doi.org/10.3390/ijms18122755] [PMID: 29257069]
[74]
Redel, B.K.; Brown, A.N.; Spate, L.D.; Whitworth, K.M.; Green, J.A.; Prather, R.S. Glycolysis in preimplantation development is partially controlled by the Warburg Effect. Mol. Reprod. Dev., 2012, 79(4), 262-271.
[http://dx.doi.org/10.1002/mrd.22017] [PMID: 22213464]
[75]
Hatzivassiliou, G.; Zhao, F.; Bauer, D.E.; Andreadis, C.; Shaw, A.N.; Dhanak, D.; Hingorani, S.R.; Tuveson, D.A.; Thompson, C.B. ATP citrate lyase inhibition can suppress tumor cell growth. Cancer Cell, 2005, 8(4), 311-321.
[http://dx.doi.org/10.1016/j.ccr.2005.09.008] [PMID: 16226706]
[76]
Pavlides, S.; Whitaker-Menezes, D.; Castello-Cros, R.; Flomenberg, N.; Witkiewicz, A.K.; Frank, P.G.; Casimiro, M.C.; Wang, C.; Fortina, P.; Addya, S.; Pestell, R.G.; Martinez-Outschoorn, U.E.; Sotgia, F.; Lisanti, M.P. The reverse Warburg effect: Aerobic glycolysis in cancer associated fibroblasts and the tumor stroma. Cell Cycle, 2009, 8(23), 3984-4001.
[http://dx.doi.org/10.4161/cc.8.23.10238] [PMID: 19923890]
[77]
Reinfeld, B.I.; Rathmell, W.K.; Kim, T.K.; Rathmell, J.C. The therapeutic implications of immunosuppressive tumor aerobic glycolysis. Cell. Mol. Immunol., 2022, 19(1), 46-58.
[http://dx.doi.org/10.1038/s41423-021-00727-3] [PMID: 34239083]
[78]
Hirpara, J.; Eu, J.Q.; Tan, J.K.M.; Wong, A.L.; Clement, M.V.; Kong, L.R.; Ohi, N.; Tsunoda, T.; Qu, J.; Goh, B.C.; Pervaiz, S. Metabolic reprogramming of oncogene-addicted cancer cells to OXPHOS as a mechanism of drug resistance. Redox Biol., 2019, 25, 101076.
[http://dx.doi.org/10.1016/j.redox.2018.101076] [PMID: 30642723]
[79]
Boese, A.C.; Kang, S. Mitochondrial metabolism-mediated redox regulation in cancer progression. Redox Biol., 2021, 42, 101870.
[http://dx.doi.org/10.1016/j.redox.2021.101870] [PMID: 33509708]
[80]
Gatenby, R.A.; Gillies, R.J. Why do cancers have high aerobic glycolysis? Nat. Rev. Cancer, 2004, 4(11), 891-899.
[http://dx.doi.org/10.1038/nrc1478] [PMID: 15516961]
[81]
Seyfried, T.N.; Mukherjee, P. Targeting energy metabolism in brain cancer: Review and hypothesis. Nutr. Metab., 2005, 2(1), 30.
[http://dx.doi.org/10.1186/1743-7075-2-30] [PMID: 16242042]
[82]
Rattan, R.; Giri, S.; Singh, A.K.; Singh, I. 5-Aminoimidazole-4-carboxamide-1-β-D-ribofuranoside inhibits cancer cell proliferation in vitro and in vivo via AMP-activated protein kinase. J. Biol. Chem., 2005, 280(47), 39582-39593.
[http://dx.doi.org/10.1074/jbc.M507443200] [PMID: 16176927]
[83]
Swinnen, J.V.; Beckers, A.; Brusselmans, K.; Organe, S.; Segers, J.; Timmermans, L.; Vanderhoydonc, F.; Deboel, L.; Derua, R.; Waelkens, E.; De Schrijver, E.; Van de Sande, T.; Noël, A.; Foufelle, F.; Verhoeven, G. Mimicry of a cellular low energy status blocks tumor cell anabolism and suppresses the malignant phenotype. Cancer Res., 2005, 65(6), 2441-2448.
[http://dx.doi.org/10.1158/0008-5472.CAN-04-3025] [PMID: 15781660]
[84]
Munir, R.; Lisec, J.; Swinnen, J.V.; Zaidi, N. Lipid metabolism in cancer cells under metabolic stress. Br. J. Cancer, 2019, 120(12), 1090-1098.
[http://dx.doi.org/10.1038/s41416-019-0451-4] [PMID: 31092908]
[85]
Igal, R.A. Stearoyl-CoA desaturase-1: A novel key player in the mechanisms of cell proliferation, programmed cell death and transformation to cancer. Carcinogenesis, 2010, 31(9), 1509-1515.
[http://dx.doi.org/10.1093/carcin/bgq131] [PMID: 20595235]
[86]
Young, R.M.; Ackerman, D.; Quinn, Z.L.; Mancuso, A.; Gruber, M.; Liu, L.; Giannoukos, D.N.; Bobrovnikova-Marjon, E.; Diehl, J.A.; Keith, B.; Simon, M.C. Dysregulated mTORC1 renders cells critically dependent on desaturated lipids for survival under tumor-like stress. Genes Dev., 2013, 27(10), 1115-1131.
[http://dx.doi.org/10.1101/gad.198630.112] [PMID: 23699409]
[87]
Krycer, J.R.; Sharpe, L.J.; Luu, W.; Brown, A.J. The Akt–SREBP nexus: Cell signaling meets lipid metabolism. Trends Endocrinol. Metab., 2010, 21(5), 268-276.
[http://dx.doi.org/10.1016/j.tem.2010.01.001] [PMID: 20117946]
[88]
Shao, W.; Espenshade, P.J. Expanding roles for SREBP in metabolism. Cell Metab., 2012, 16(4), 414-419.
[http://dx.doi.org/10.1016/j.cmet.2012.09.002] [PMID: 23000402]
[89]
Mashima, T.; Seimiya, H.; Tsuruo, T. De novo fatty-acid synthesis and related pathways as molecular targets for cancer therapy. Br. J. Cancer, 2009, 100(9), 1369-1372.
[http://dx.doi.org/10.1038/sj.bjc.6605007] [PMID: 19352381]
[90]
Yan, S.; Cui, S.; Ke, K.; Zhao, B.; Liu, X.; Yue, S.; Wang, P. Hyperspectral stimulated raman scattering microscopy unravels aberrant accumulation of saturated fat in human liver cancer. Anal. Chem., 2018, 90(11), 6362-6366.
[http://dx.doi.org/10.1021/acs.analchem.8b01312] [PMID: 29757615]
[91]
Kuhajda, F.P. Fatty-acid synthase and human cancer: new perspectives on its role in tumor biology. Nutrition, 2000, 16(3), 202-208.
[http://dx.doi.org/10.1016/S0899-9007(99)00266-X] [PMID: 10705076]
[92]
Joyce, J.G.; Tung, J.S.; Przysiecki, C.T.; Cook, J.C.; Lehman, E.D.; Sands, J.A.; Jansen, K.U.; Keller, P.M. The L1 major capsid protein of human papillomavirus type 11 recombinant virus-like particles interacts with heparin and cell-surface glycosaminoglycans on human keratinocytes. J. Biol. Chem., 1999, 274(9), 5810-5822.
[http://dx.doi.org/10.1074/jbc.274.9.5810] [PMID: 10026203]
[93]
Kridel, S.J.; Axelrod, F.; Rozenkrantz, N.; Smith, J.W. Orlistat is a novel inhibitor of fatty acid synthase with antitumor activity. Cancer Res., 2004, 64(6), 2070-2075.
[http://dx.doi.org/10.1158/0008-5472.CAN-03-3645] [PMID: 15026345]
[94]
Sounni, N.E.; Cimino, J.; Blacher, S.; Primac, I.; Truong, A.; Mazzucchelli, G.; Paye, A.; Calligaris, D.; Debois, D.; De Tullio, P.; Mari, B.; De Pauw, E.; Noel, A. Blocking lipid synthesis overcomes tumor regrowth and metastasis after antiangiogenic therapy withdrawal. Cell Metab., 2014, 20(2), 280-294.
[http://dx.doi.org/10.1016/j.cmet.2014.05.022] [PMID: 25017943]
[95]
Pascual, G.; Avgustinova, A.; Mejetta, S.; Martín, M.; Castellanos, A.; Attolini, C.S.O.; Berenguer, A.; Prats, N.; Toll, A.; Hueto, J.A.; Bescós, C.; Di Croce, L.; Benitah, S.A. Targeting metastasis-initiating cells through the fatty acid receptor CD36. Nature, 2017, 541(7635), 41-45.
[http://dx.doi.org/10.1038/nature20791] [PMID: 27974793]
[96]
Münger, K.; Howley, P.M. Human papillomavirus immortalization and transformation functions. Virus Res., 2002, 89(2), 213-228.
[http://dx.doi.org/10.1016/S0168-1702(02)00190-9] [PMID: 12445661]
[97]
Han, J.; Zhang, L.; Guo, H.; Wysham, W.Z.; Roque, D.R.; Willson, A.K.; Sheng, X.; Zhou, C.; Bae-Jump, V.L. Glucose promotes cell proliferation, glucose uptake and invasion in endometrial cancer cells via AMPK/mTOR/S6 and MAPK signaling. Gynecol. Oncol., 2015, 138(3), 668-675.
[http://dx.doi.org/10.1016/j.ygyno.2015.06.036] [PMID: 26135947]
[98]
Song, K.; Li, M.; Xu, X.; Xuan, L.; Huang, G.; Liu, Q. Resistance to chemotherapy is associated with altered glucose metabolism in acute myeloid leukemia. Oncol. Lett., 2016, 12(1), 334-342.
[http://dx.doi.org/10.3892/ol.2016.4600] [PMID: 27347147]
[99]
Mazurek, S.; Boschek, C.B.; Hugo, F.; Eigenbrodt, E. Pyruvate kinase type M2 and its role in tumor growth and spreading. Semin. Cancer Biol., 2005, 15(4), 300-308.
[http://dx.doi.org/10.1016/j.semcancer.2005.04.009] [PMID: 15908230]
[100]
Yuan, Y.; Cai, X.; Shen, F.; Ma, F. HPV post-infection microenvironment and cervical cancer. Cancer Lett., 2021, 497, 243-254.
[http://dx.doi.org/10.1016/j.canlet.2020.10.034] [PMID: 33122098]
[101]
Ilhan, Z.E.; Łaniewski, P.; Thomas, N.; Roe, D.J.; Chase, D.M.; Herbst-Kralovetz, M.M. Deciphering the complex interplay between microbiota, HPV, inflammation and cancer through cervicovaginal metabolic profiling. EBioMedicine, 2019, 44, 675-690.
[http://dx.doi.org/10.1016/j.ebiom.2019.04.028] [PMID: 31027917]
[102]
Sitarz, K.; Czamara, K.; Bialecka, J.; Klimek, M.; Zawilinska, B.; Szostek, S.; Kaczor, A. HPV infection significantly accelerates glycogen metabolism in cervical cells with large nuclei: Raman microscopic study with subcellular resolution. Int. J. Mol. Sci., 2020, 21(8), 2667.
[http://dx.doi.org/10.3390/ijms21082667] [PMID: 32290479]
[103]
Castro-Muñoz, L.J.; Manzo-Merino, J.; Muñoz-Bello, J.O.; Olmedo-Nieva, L.; Cedro-Tanda, A.; Alfaro-Ruiz, L.A.; Hidalgo-Miranda, A.; Madrid-Marina, V.; Lizano, M. The Human Papillomavirus (HPV) E1 protein regulates the expression of cellular genes involved in immune response. Sci. Rep., 2019, 9(1), 13620.
[http://dx.doi.org/10.1038/s41598-019-49886-4] [PMID: 31541186]
[104]
He, M.; Jin, Q.; Chen, C.; Liu, Y.; Ye, X.; Jiang, Y.; Ji, F.; Qian, H.; Gan, D.; Yue, S.; Zhu, W.; Chen, T. The miR-186-3p/EREG axis orchestrates tamoxifen resistance and aerobic glycolysis in breast cancer cells. Oncogene, 2019, 38(28), 5551-5565.
[http://dx.doi.org/10.1038/s41388-019-0817-3] [PMID: 30967627]
[105]
Lee, I.H.; Sohn, M.; Lim, H.J.; Yoon, S.; Oh, H.; Shin, S.; Shin, J.H.; Oh, S-H.; Kim, J.; Lee, D.K.; Noh, D.Y.; Bae, D.S.; Seong, J.K.; Bae, Y.S. Ahnak functions as a tumor suppressor via modulation of TGFβ/Smad signaling pathway. Oncogene, 2014, 33(38), 4675-4684.
[http://dx.doi.org/10.1038/onc.2014.69] [PMID: 24662814]
[106]
Cruz-Gregorio, A.; Manzo-Merino, J.; Gonzaléz-García, M.C.; Pedraza-Chaverri, J.; Medina-Campos, O.N.; Valverde, M.; Rojas, E.; Rodríguez-Sastre, M.A.; García-Cuellar, C.M.; Lizano, M. Human papillomavirus types 16 and 18 early-expressed proteins differentially modulate the cellular redox state and DNA damage. Int. J. Biol. Sci., 2018, 14(1), 21-35.
[http://dx.doi.org/10.7150/ijbs.21547] [PMID: 29483822]
[107]
Wang, T.; Liu, H.; Lian, G.; Zhang, S-Y.; Wang, X.; Jiang, C. HIF1α-induced glycolysis metabolism is essential to the activation of inflammatory macrophages. Mediators Inflamm., 2017, 2017, 1-10.
[http://dx.doi.org/10.1155/2017/3102737]
[108]
Jung, S.N.; Yang, W.K.; Kim, J.; Kim, H.S.; Kim, E.J.; Yun, H.; Park, H.; Kim, S.S.; Choe, W.; Kang, I.; Ha, J. Reactive oxygen species stabilize hypoxia-inducible factor-1 alpha protein and stimulate transcriptional activity via AMP-activated protein kinase in DU145 human prostate cancer cells. Carcinogenesis, 2008, 29(4), 713-721.
[http://dx.doi.org/10.1093/carcin/bgn032] [PMID: 18258605]
[109]
Lai, D.; Tan, C.L.; Gunaratne, J.; Quek, L.S.; Nei, W.; Thierry, F.; Bellanger, S. Localization of HPV-18 E2 at mitochondrial membranes induces ROS release and modulates host cell metabolism. PLoS One, 2013, 8(9), e75625.
[http://dx.doi.org/10.1371/journal.pone.0075625] [PMID: 24086592]
[110]
Ilahi, N.E.; Bhatti, A. Impact of HPV E5 on viral life cycle via EGFR signaling. Microb. Pathog., 2020, 139, 103923.
[http://dx.doi.org/10.1016/j.micpath.2019.103923] [PMID: 31836496]
[111]
An, Z.; Aksoy, O.; Zheng, T.; Fan, Q.W.; Weiss, W.A. Epidermal growth factor receptor and EGFRvIII in glioblastoma: signaling pathways and targeted therapies. Oncogene, 2018, 37(12), 1561-1575.
[http://dx.doi.org/10.1038/s41388-017-0045-7] [PMID: 29321659]
[112]
Valle-Mendiola, A.; Soto-Cruz, I. Energy metabolism in cancer: The roles of STAT3 and STAT5 in the regulation of metabolism-related genes. Cancers, 2020, 12(1), 124.
[http://dx.doi.org/10.3390/cancers12010124] [PMID: 31947710]
[113]
Xie, Y.; Shi, X.; Sheng, K.; Han, G.; Li, W.; Zhao, Q.; Jiang, B.; Feng, J.; Li, J.; Gu, Y. PI3K/Akt signaling transduction pathway, erythropoiesis and glycolysis in hypoxia (Review). Mol. Med. Rep., 20189, 19(2), 783-791.
[http://dx.doi.org/10.3892/mmr.2018.9713] [PMID: 30535469]
[114]
Papa, S.; Choy, P.M.; Bubici, C. The ERK and JNK pathways in the regulation of metabolic reprogramming. Oncogene, 2019, 38(13), 2223-2240.
[http://dx.doi.org/10.1038/s41388-018-0582-8] [PMID: 30487597]
[115]
Blair, D.; Dufort, F.J.; Chiles, T.C. Protein kinase Cβ is critical for the metabolic switch to glycolysis following B-cell antigen receptor engagement. Biochem. J., 2012, 448(1), 165-169.
[http://dx.doi.org/10.1042/BJ20121225] [PMID: 22994860]
[116]
Xu, Q.; Zhang, Q.; Ishida, Y.; Hajjar, S.; Tang, X.; Shi, H.; Dang, C.V.; Le, A.D. EGF induces epithelial-mesenchymal transition and cancer stem-like cell properties in human oral cancer cells via promoting Warburg effect. Oncotarget, 2017, 8(6), 9557-9571.
[http://dx.doi.org/10.18632/oncotarget.13771] [PMID: 27926487]
[117]
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]
[118]
Chandel, V.; Raj, S.; Kumar, P.; Gupta, S.; Dhasmana, A.; Kesari, K.K.; Ruokolainen, J.; Mehra, P.; Das, B.C.; Kamal, M.A.; Kumar, D. Metabolic regulation in HPV associated head and neck squamous cell carcinoma. Life Sci., 2020, 258, 118236.
[http://dx.doi.org/10.1016/j.lfs.2020.118236] [PMID: 32795537]
[119]
Jang, M.; Rhee, J.; Jang, D.H.; Kim, S.S. Gene expression profiles are altered in human papillomavirus-16 E6 D25E-expressing cell lines. Virol. J., 2011, 8(1), 453.
[http://dx.doi.org/10.1186/1743-422X-8-453] [PMID: 21943319]
[120]
Thomas, M.C.; Chiang, C.M. E6 oncoprotein represses p53-dependent gene activation in vitro inhibition of protein acetylation independently of inducing p53 degradation. Mol. Cell, 2005, 17(2), 251-264.
[http://dx.doi.org/10.1016/j.molcel.2004.12.016] [PMID: 15664194]
[121]
Green, D.R.; Chipuk, J.E. p53 and Metabolism: Inside the TIGAR. Cell, 2006, 126(1), 30-32.
[http://dx.doi.org/10.1016/j.cell.2006.06.032] [PMID: 16839873]
[122]
Schwartzenberg-Bar-Yoseph, F.; Armoni, M.; Karnieli, E. The tumor suppressor p53 down-regulates glucose transporters GLUT1 and GLUT4 gene expression. Cancer Res., 2004, 64(7), 2627-2633.
[http://dx.doi.org/10.1158/0008-5472.CAN-03-0846] [PMID: 15059920]
[123]
Choy, M.K.; Movassagh, M.; Bennett, M.R.; Foo, R.S.Y. PKB/Akt activation inhibits p53-mediated HIF1A degradation that is independent of MDM2. J. Cell. Physiol., 2010, 222(3), 635-639.
[http://dx.doi.org/10.1002/jcp.21980] [PMID: 19950214]
[124]
Leiprecht, N.; Munoz, C.; Alesutan, I.; Siraskar, G.; Sopjani, M.; Föller, M.; Stubenrauch, F.; Iftner, T.; Lang, F. Regulation of Na+-coupled glucose carrier SGLT1 by human papillomavirus 18 E6 protein. Biochem. Biophys. Res. Commun., 2011, 404(2), 695-700.
[http://dx.doi.org/10.1016/j.bbrc.2010.12.044] [PMID: 21156162]
[125]
Ganapathy, V.; Thangaraju, M.; Prasad, P.D. Nutrient transporters in cancer: Relevance to Warburg hypothesis and beyond. Pharmacol. Ther., 2009, 121(1), 29-40.
[http://dx.doi.org/10.1016/j.pharmthera.2008.09.005] [PMID: 18992769]
[126]
Gonzalez-Menendez, P.; Hevia, D.; Mayo, J.C.; Sainz, R.M. The dark side of glucose transporters in prostate cancer: Are they a new feature to characterize carcinomas? Int. J. Cancer, 2018, 142(12), 2414-2424.
[http://dx.doi.org/10.1002/ijc.31165] [PMID: 29159872]
[127]
Medina, R.A.; Owen, G. Glucose transporters: Expression, regulation and cancer. Biol. Res., 2002, 35(1), 9-26.
[http://dx.doi.org/10.4067/S0716-97602002000100004] [PMID: 12125211]
[128]
Weihua, Z.; Tsan, R.; Huang, W.C.; Wu, Q.; Chiu, C.H.; Fidler, I.J.; Hung, M.C. Survival of cancer cells is maintained by EGFR independent of its kinase activity. Cancer Cell, 2008, 13(5), 385-393.
[http://dx.doi.org/10.1016/j.ccr.2008.03.015] [PMID: 18455122]
[129]
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., 2010, 107(16), 7461-7466.
[http://dx.doi.org/10.1073/pnas.1002459107] [PMID: 20351271]
[130]
Plaitakis, A.; Kalef-Ezra, E.; Kotzamani, D.; Zaganas, I.; Spanaki, C. The glutamate dehydrogenase pathway and its roles in cell and tissue biology in health and disease. Biology, 2017, 6(4), 11.
[http://dx.doi.org/10.3390/biology6010011] [PMID: 28208702]
[131]
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.
[http://dx.doi.org/10.3892/ijo.2017.3979] [PMID: 28498475]
[132]
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.
[http://dx.doi.org/10.1186/1750-9378-6-18] [PMID: 22032288]
[133]
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., 2003, 100(14), 8211-8216.
[http://dx.doi.org/10.1073/pnas.1435900100] [PMID: 12821782]
[134]
Spangle, J.M.; Münger, K. The human papillomavirus type 16 E6 oncoprotein activates mTORC1 signaling and increases protein synthesis. J. Virol., 2010, 84(18), 9398-9407.
[http://dx.doi.org/10.1128/JVI.00974-10] [PMID: 20631133]
[135]
Semenza, G.L. HIF-1: Upstream and downstream of cancer metabolism. Curr. Opin. Genet. Dev., 2010, 20(1), 51-56.
[http://dx.doi.org/10.1016/j.gde.2009.10.009] [PMID: 19942427]
[136]
Semenza, G.L. Defining the role of hypoxia-inducible factor 1 in cancer biology and therapeutics. Oncogene, 2010, 29(5), 625-634.
[http://dx.doi.org/10.1038/onc.2009.441] [PMID: 19946328]
[137]
Sarbassov, D.D.; Ali, S.M.; Sengupta, S.; Sheen, J.H.; Hsu, P.P.; Bagley, A.F.; Markhard, A.L.; Sabatini, D.M. Prolonged rapamycin treatment inhibits mTORC2 assembly and Akt/PKB. Mol. Cell, 2006, 22(2), 159-168.
[http://dx.doi.org/10.1016/j.molcel.2006.03.029] [PMID: 16603397]
[138]
Wong, N.; Ojo, D.; Yan, J.; Tang, D. PKM2 contributes to cancer metabolism. Cancer Lett., 2015, 356(2), 184-191.
[http://dx.doi.org/10.1016/j.canlet.2014.01.031] [PMID: 24508027]
[139]
Menges, C.W.; Baglia, L.A.; Lapoint, R.; McCance, D.J. Human papillomavirus type 16 E7 up-regulates AKT activity through the retinoblastoma protein. Cancer Res., 2006, 66(11), 5555-5559.
[http://dx.doi.org/10.1158/0008-5472.CAN-06-0499] [PMID: 16740689]
[140]
Zwerschke, W.; Mazurek, S.; Massimi, P.; Banks, L.; Eigenbrodt, E.; Jansen-Dürr, P. Modulation of type M 2 pyruvate kinase activity by the human papillomavirus type 16 E7 oncoprotein. Proc. Natl. Acad. Sci., 1999, 96(4), 1291-1296.
[http://dx.doi.org/10.1073/pnas.96.4.1291] [PMID: 9990017]
[141]
Zwerschke, W.; Mannhardt, B.; Massimi, P.; Nauenburg, S.; Pim, D.; Nickel, W.; Banks, L.; Reuser, A.J.; Jansen-Dürr, P. Allosteric activation of acid α-glucosidase by the human papillomavirus E7 protein. J. Biol. Chem., 2000, 275(13), 9534-9541.
[http://dx.doi.org/10.1074/jbc.275.13.9534] [PMID: 10734102]
[142]
Kirschberg, M.; Heuser, S.; Marcuzzi, G.P.; Hufbauer, M.; Seeger, J.M.; Đukić, A.; Tomaić, V.; Majewski, S.; Wagner, S.; Wittekindt, C.; Würdemann, N.; Klussmann, J.P.; Quaas, A.; Kashkar, H.; Akgül, B. ATP synthase modulation leads to an increase of spare respiratory capacity in HPV associated cancers. Sci. Rep., 2020, 10(1), 17339.
[http://dx.doi.org/10.1038/s41598-020-74311-6] [PMID: 33060693]
[143]
Christofk, H.R.; Vander Heiden, M.G.; Harris, M.H.; Ramanathan, A.; Gerszten, R.E.; Wei, R.; Fleming, M.D.; Schreiber, S.L.; Cantley, L.C. The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth. Nature, 2008, 452(7184), 230-233.
[http://dx.doi.org/10.1038/nature06734] [PMID: 18337823]
[144]
Zeng, Q.; Chen, J.; Li, Y.; Werle, K.D.; Zhao, R-X.; Quan, C-S.; Wang, Y-S.; Zhai, Y-X.; Wang, J-W.; Youssef, M.; Cui, R.; Liang, J.; Genovese, N.; Chow, L.T.; Li, Y-L.; Xu, Z-X. LKB1 inhibits HPV-associated cancer progression by targeting cellular metabolism. Oncogene, 2017, 36(9), 1245-1255.
[http://dx.doi.org/10.1038/onc.2016.290] [PMID: 27546620]
[145]
Zhuo, B.; Li, Y.; Li, Z.; Qin, H.; Sun, Q.; Zhang, F.; Shen, Y.; Shi, Y.; Wang, R. PI3K/Akt signaling mediated Hexokinase-2 expression inhibits cell apoptosis and promotes tumor growth in pediatric osteosarcoma. Biochem. Biophys. Res. Commun., 2015, 464(2), 401-406.
[http://dx.doi.org/10.1016/j.bbrc.2015.06.092] [PMID: 26116768]
[146]
Hu, C.; Liu, T.; Han, C.; Xuan, Y.; Jiang, D.; Sun, Y.; Zhang, X.; Zhang, W.; Xu, Y.; Liu, Y.; Pan, J.; Wang, J.; Fan, J.; Che, Y.; Huang, Y.; Zhang, J.; Ding, J.; Yang, S.; Yang, K. HPV E6/E7 promotes aerobic glycolysis in cervical cancer by regulating IGF2BP2 to stabilize m 6 A-MYC expression. Int. J. Biol. Sci., 2022, 18(2), 507-521.
[http://dx.doi.org/10.7150/ijbs.67770] [PMID: 35002506]
[147]
Hoppe-Seyler, K.; Honegger, A.; Bossler, F.; Sponagel, J.; Bulkescher, J.; Lohrey, C.; Hoppe-Seyler, F. Viral E6/E7 oncogene and cellular hexokinase 2 expression in HPV-positive cancer cell lines. Oncotarget, 2017, 8(63), 106342-106351.
[http://dx.doi.org/10.18632/oncotarget.22463] [PMID: 29290953]
[148]
Jin, L.H.; Wei, C. Role of microRNAs in the Warburg effect and mitochondrial metabolism in cancer. Asian Pac. J. Cancer Prev., 2014, 15(17), 7015-7019.
[http://dx.doi.org/10.7314/APJCP.2014.15.17.7015] [PMID: 25227784]
[149]
Gao, P.; Sun, L.; He, X.; Cao, Y.; Zhang, H. MicroRNAs and the warburg effect: New players in an old arena. Curr. Gene Ther., 2012, 12(4), 285-291.
[http://dx.doi.org/10.2174/156652312802083620] [PMID: 22856603]
[150]
Wei, Z.; Cui, L.; Mei, Z.; Liu, M.; Zhang, D. miR-181a mediates metabolic shift in colon cancer cells via the PTEN/AKT pathway. FEBS Lett., 2014, 588(9), 1773-1779.
[http://dx.doi.org/10.1016/j.febslet.2014.03.037] [PMID: 24685694]
[151]
Masui, K.; Tanaka, K.; Akhavan, D.; Babic, I.; Gini, B.; Matsutani, T.; Iwanami, A.; Liu, F.; Villa, G.R.; Gu, Y.; Campos, C.; Zhu, S.; Yang, H.; Yong, W.H.; Cloughesy, T.F.; Mellinghoff, I.K.; Cavenee, W.K.; Shaw, R.J.; Mischel, P.S. mTOR complex 2 controls glycolytic metabolism in glioblastoma through FoxO acetylation and upregulation of c-Myc. Cell Metab., 2013, 18(5), 726-739.
[http://dx.doi.org/10.1016/j.cmet.2013.09.013] [PMID: 24140020]
[152]
Zine El Abidine, A.; Tomaić, V.; Bel Haj Rhouma, R.; Massimi, P.; Guizani, I.; Boubaker, S.; Ennaifer, E.; Banks, L. A naturally occurring variant of HPV-16 E7 exerts increased transforming activity through acquisition of an additional phospho-acceptor site. Virology, 2017, 500, 218-225.
[http://dx.doi.org/10.1016/j.virol.2016.10.023] [PMID: 27829177]
[153]
Wang, S.; Li, J.; Xie, J.; Liu, F.; Duan, Y.; Wu, Y.; Huang, S.; He, X.; Wang, Z.; Wu, X. Programmed death ligand 1 promotes lymph node metastasis and glucose metabolism in cervical cancer by activating integrin β4/SNAI1/SIRT3 signaling pathway. Oncogene, 2018, 37(30), 4164-4180.
[http://dx.doi.org/10.1038/s41388-018-0252-x] [PMID: 29706653]
[154]
Chai, Z.; Yang, Y.; Gu, Z.; Cai, X.; Ye, W.; Kong, L.; Qiu, X.; Ying, L.; Wang, Z.; Wang, L. Recombinant viral capsid protein L2 (rVL2) of HPV 16 suppresses cell proliferation and glucose metabolism via ITGB7/C/EBPβ signaling pathway in cervical cancer cell lines. OncoTargets Ther., 2019, 12, 10415-10425.
[http://dx.doi.org/10.2147/OTT.S228631] [PMID: 31819523]
[155]
Sitarz, K.; Czamara, K.; Bialecka, J.; Klimek, M.; Szostek, S.; Kaczor, A. Dual switch in lipid metabolism in cervical epithelial cells during dysplasia development observed using raman microscopy and molecular methods. Cancers, 2021, 13(9), 1997.
[http://dx.doi.org/10.3390/cancers13091997] [PMID: 33919178]
[156]
Guri, Y.; Colombi, M.; Dazert, E.; Hindupur, S.K.; Roszik, J.; Moes, S.; Jenoe, P.; Heim, M.H.; Riezman, I.; Riezman, H.; Hall, M.N. mTORC2 promotes tumorigenesis via lipid synthesis. Cancer Cell, 2017, 32(6), 807-823.e12.
[http://dx.doi.org/10.1016/j.ccell.2017.11.011] [PMID: 29232555]
[157]
Carracedo, A.; Cantley, L.C.; Pandolfi, P.P. Cancer metabolism: Fatty acid oxidation in the limelight. Nat. Rev. Cancer, 2013, 13(4), 227-232.
[http://dx.doi.org/10.1038/nrc3483] [PMID: 23446547]
[158]
Wang, T.; Fahrmann, J.F.; Lee, H.; Li, Y.J.; Tripathi, S.C.; Yue, C.; Zhang, C.; Lifshitz, V.; Song, J.; Yuan, Y.; Somlo, G.; Jandial, R.; Ann, D.; Hanash, S.; Jove, R.; Yu, H. JAK/STAT3-regulated fatty acid β-oxidation is critical for breast cancer stem cell self-renewal and chemoresistance. Cell Metab., 2018, 27(6), 1357.
[http://dx.doi.org/10.1016/j.cmet.2018.04.018] [PMID: 29874570]
[159]
Zietkowski, D.; deSouza, N.M.; Davidson, R.L.; Payne, G.S. Characterisation of mobile lipid resonances in tissue biopsies from patients with cervical cancer and correlation with cytoplasmic lipid droplets. NMR Biomed., 2013, 26(9), 1096-1102.
[http://dx.doi.org/10.1002/nbm.2923] [PMID: 23417787]
[160]
Sharma, A.; Jha, A.K.; Mishra, S.; Jain, A.; Chauhan, B.S.; Kathuria, M.; Rawat, K.S.; Gupta, N.M.; Tripathi, R.; Mitra, K.; Sachdev, M.; Bhatt, M.L.B.; Goel, A. Imaging and quantitative detection of lipid droplets by yellow fluorescent probes in liver sections of plasmodium infected mice and third stage human cervical cancer tissues. Bioconjug. Chem., 2018, 29(11), 3606-3613.
[http://dx.doi.org/10.1021/acs.bioconjchem.8b00552] [PMID: 30247899]
[161]
Mondal, S.; Roy, D.; Sarkar, B.S.; Jin, L.; Jung, D.; Zhang, S.; Kalogera, E.; Staub, J.; Wang, Y.; Xuyang, W.; Khurana, A.; Chien, J.; Telang, S.; Chesney, J.; Tapolsky, G.; Petras, D.; Shridhar, V. Therapeutic targeting of PFKFB3 with a novel glycolytic inhibitor PFK158 promotes lipophagy and chemosensitivity in gynecologic cancers. Int. J. Cancer, 2019, 144(1), 178-189.
[http://dx.doi.org/10.1002/ijc.31868] [PMID: 30226266]
[162]
Shang, C.; Wang, W.; Liao, Y.; Chen, Y.; Liu, T.; Du, Q.; Huang, J.; Liang, Y.; Liu, J.; Zhao, Y.; Guo, L.; Hu, Z.; Yao, S. LNMICC promotes nodal metastasis of cervical cancer by reprogramming fatty acid metabolism. Cancer Res., 2018, 78(4), 877-890.
[http://dx.doi.org/10.1158/0008-5472.CAN-17-2356] [PMID: 29229603]
[163]
Bravo, I.G.; Crusius, K.; Alonso, A. The E5 protein of the human papillomavirus type 16 modulates composition and dynamics of membrane lipids in keratinocytes. Arch. Virol., 2005, 150(2), 231-246.
[http://dx.doi.org/10.1007/s00705-004-0420-x] [PMID: 15503216]
[164]
Ni, K.; Wang, D.; Xu, H.; Mei, F.; Wu, C.; Liu, Z.; Zhou, B. miR-21 promotes non-small cell lung cancer cells growth by regulating fatty acid metabolism. Cancer Cell Int., 2019, 19(1), 219.
[http://dx.doi.org/10.1186/s12935-019-0941-8] [PMID: 31462892]
[165]
Lopaschuk, G.D.; Ussher, J.R.; Folmes, C.D.L.; Jaswal, J.S.; Stanley, W.C. Myocardial fatty acid metabolism in health and disease. Physiol. Rev., 2010, 90(1), 207-258.
[http://dx.doi.org/10.1152/physrev.00015.2009] [PMID: 20086077]
[166]
Ma, D.; Huang, Y.; Song, S. Inhibiting the HPV16 oncogene-mediated glycolysis sensitizes human cervical carcinoma cells to 5-fluorouracil. OncoTargets Ther., 2019, 12, 6711-6720.
[http://dx.doi.org/10.2147/OTT.S205334] [PMID: 31695407]
[167]
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.
[http://dx.doi.org/10.1158/1535-7163.MCT-12-1188] [PMID: 23883584]
[168]
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.
[http://dx.doi.org/10.1038/msb.2012.25] [PMID: 22864381]
[169]
Martinho, O.; Silva-Oliveira, R.; Cury, F.P.; Barbosa, A.M.; Granja, S.; Evangelista, A.F.; Marques, F.; Miranda-Gonçalves, V.; Cardoso-Carneiro, D.; de Paula, F.E.; Zanon, M.; Scapulatempo-Neto, C.; Moreira, M.A.R.; Baltazar, F.; Longatto-Filho, A.; Reis, R.M. HER family receptors are important theranostic biomarkers for cervical cancer: Blocking glucose metabolism enhances the therapeutic effect of HER inhibitors. Theranostics, 2017, 7(3), 717-732.
[http://dx.doi.org/10.7150/thno.17154] [PMID: 28255362]
[170]
Coppock, J.D.; Lee, J.H. mTOR, metabolism, and the immune response in HPV-positive head and neck squamous cell cancer. World J. Otorhinolaryngol. Head Neck Surg., 2016, 2(2), 76-83.
[http://dx.doi.org/10.1016/j.wjorl.2016.05.010] [PMID: 29204551]
[171]
Lucido, C.T.; Callejas-Valera, J.L.; Colbert, P.L.; Vermeer, D.W.; Miskimins, W.K.; Spanos, W.C.; Vermeer, P.D. β2-Adrenergic receptor modulates mitochondrial metabolism and disease progression in recurrent/metastatic HPV(+) HNSCC. Oncogenesis, 2018, 7(10), 81.
[http://dx.doi.org/10.1038/s41389-018-0090-2] [PMID: 30297705]
[172]
Lucido, C.; Miskimins, W.; Vermeer, P. Propranolol promotes glucose dependence and synergizes with dichloroacetate for anti-cancer activity in HNSCC. Cancers, 2018, 10(12), 476.
[http://dx.doi.org/10.3390/cancers10120476] [PMID: 30513596]
[173]
Liu, Z.; Zhu, W.; Kong, X.; Chen, X.; Sun, X.; Zhang, W.; Zhang, R. Tanshinone IIA inhibits glucose metabolism leading to apoptosis in cervical cancer. Oncol. Rep., 2019, 42(5), 1893-1903.
[http://dx.doi.org/10.3892/or.2019.7294] [PMID: 31485631]
[174]
Gao, R.; Wu, X.; Huang, Z.; Wang, B.; Li, F.; Xu, H.; Ran, L. Anti-tumor effect of aloe-emodin on cervical cancer cells was associated with human papillomavirus E6/E7 and glucose metabolism. OncoTargets Ther., 2019, 12, 3713-3721.
[http://dx.doi.org/10.2147/OTT.S182405] [PMID: 31190872]
[175]
Celegato, M.; Messa, L.; Goracci, L.; Mercorelli, B.; Bertagnin, C.; Spyrakis, F.; Suarez, I.; Cousido-Siah, A.; Travé, G.; Banks, L.; Cruciani, G.; Palù, G.; Loregian, A. A novel small-molecule inhibitor of the human papillomavirus E6-p53 interaction that reactivates p53 function and blocks cancer cells growth. Cancer Lett., 2020, 470, 115-125.
[http://dx.doi.org/10.1016/j.canlet.2019.10.046] [PMID: 31693922]
[176]
Gu, Z.; Zhang, H.; Guo, X.; Cao, Y. Enhanced glycogen metabolism supports the survival and proliferation of HPV-infected keratinocytes in condylomata acuminata. J. Invest. Dermatol., 2020, 140(8), 1513-1523.e5.
[http://dx.doi.org/10.1016/j.jid.2020.01.010] [PMID: 32004566]
[177]
Sattler, U.G.A.; Mueller-Klieser, W. The anti-oxidant capacity of tumour glycolysis. Int. J. Radiat. Biol., 2009, 85(11), 963-971.
[http://dx.doi.org/10.3109/09553000903258889] [PMID: 19895273]
[178]
Trachootham, D.; Alexandre, J.; Huang, P. Targeting cancer cells by ROS-mediated mechanisms: A radical therapeutic approach? Nat. Rev. Drug Discov., 2009, 8(7), 579-591.
[http://dx.doi.org/10.1038/nrd2803] [PMID: 19478820]
[179]
Hensley, C.T.; Faubert, B.; Yuan, Q.; Lev-Cohain, N.; Jin, E.; Kim, J.; Jiang, L.; Ko, B.; Skelton, R.; Loudat, L.; Wodzak, M.; Klimko, C.; McMillan, E.; Butt, Y.; Ni, M.; Oliver, D.; Torrealba, J.; Malloy, C.R.; Kernstine, K.; Lenkinski, R.E.; DeBerardinis, R.J. Metabolic heterogeneity in human lung tumors. Cell, 2016, 164(4), 681-694.
[http://dx.doi.org/10.1016/j.cell.2015.12.034] [PMID: 26853473]

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