1932

Abstract

Viruses are fundamental tools in cancer research. They were used to discover the first oncogenes in the 1970s, and they are now being modified for use as antitumor therapeutics. Key to both of these oncogenic and oncolytic properties is the ability of viruses to rewire host cell metabolism. In this review, we describe how viral oncogenes alter metabolism to increase the synthesis of macromolecules necessary for both viral replication and tumor growth. We then describe how understanding the specific metabolic requirements of virus-infected cells can help guide strategies to improve the efficacy of oncolytic viruses, and we highlight immunometabolism and tumor microenvironment research that could also increase the therapeutic benefits of oncolytic viruses. We also describe how studies describing the therapeutic effects of dietary nutrient restriction in cancer can suggest new avenues for research into antiviral therapeutics.

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2022-04-11
2024-06-25
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Literature Cited

  1. Ackermann WW, Kleinschmidt E. 1951. The role of l-methionine in virus propagation. J. Exp. Med. 93:4337–43
    [Google Scholar]
  2. Andersson-Anvret M, Forsby N, Klein G, Henle W. 1977. Relationship between the Epstein-Barr virus and undifferentiated nasopharyngeal carcinoma: correlated nucleic acid hybridization and histopathological examination. Int. J. Cancer 20:4486–94
    [Google Scholar]
  3. Andtbacka RHI, Kaufman HL, Collichio F, Amatruda T, Senzer N et al. 2015. Talimogene laherparepvec improves durable response rate in patients with advanced melanoma. J. Clin. Oncol. 33:252780–88
    [Google Scholar]
  4. Bárcena C, Quirós PM, Durand S, Mayoral P, Rodríguez F et al. 2018. Methionine restriction extends lifespan in progeroid mice and alters lipid and bile acid metabolism. Cell Rep 24:92392–403
    [Google Scholar]
  5. Beck S, Zhu Z, Oliveira MF, Smith DM, Rich JN et al. 2019. Mechanism of action of methotrexate against Zika virus. Viruses 11:4338
    [Google Scholar]
  6. Ben-Sahra I, Howell JJ, Asara JM, Manning BD. 2013. Stimulation of de novo pyrimidine synthesis by growth signaling through mTOR and S6K1. Science 339:61251323–28
    [Google Scholar]
  7. Ben-Sahra I, Hoxhaj G, Ricoult SJH, Asara JM, Manning BD. 2016. mTORC1 induces purine synthesis through control of the mitochondrial tetrahydrofolate cycle. Science 351:6274728–33
    [Google Scholar]
  8. Berrios C, Padi M, Keibler MA, Park DE, Molla V et al. 2016. Merkel cell polyomavirus small T antigen promotes pro-glycolytic metabolic perturbations required for transformation. PLOS Pathog 12:11e1006020
    [Google Scholar]
  9. Bodily JM, Mehta KPM, Laimins LA. 2011. Human papillomavirus E7 enhances hypoxia-inducible factor 1–mediated transcription by inhibiting binding of histone deacetylases. Cancer Res 71:31187–95
    [Google Scholar]
  10. Boerner JL, Danielsen A, Maihle NJ 2003. Ligand-independent oncogenic signaling by the epidermal growth factor receptor: v-ErbB as a paradigm. Exp. Cell Res. 284:1111–21
    [Google Scholar]
  11. Cantley LC, Whitman M, Chahwala S, Fleischman L, Kaplan DR et al. 1986. Oncogenes and phosphatidyl-inositol turnover. Ann. N.Y. Acad. Sci. 488:481–90
    [Google Scholar]
  12. Carroll PA, Diolaiti D, McFerrin L, Gu H, Djukovic D et al. 2015. Deregulated Myc requires MondoA/Mlx for metabolic reprogramming and tumorigenesis. Cancer Cell 27:2271–85
    [Google Scholar]
  13. Castaño-Martinez T, Schumacher F, Schumacher S, Kochlik B, Weber D et al. 2019. Methionine restriction prevents onset of type 2 diabetes in NZO mice. FASEB J 33:67092–102
    [Google Scholar]
  14. Cerezo M, Rocchi S. 2020. Cancer cell metabolic reprogramming: a keystone for the response to immunotherapy. Cell Death Dis 11:11964
    [Google Scholar]
  15. Chang CL, Ma B, Pang X, Wu TC, Hung CF. 2009. Treatment with cyclooxygenase-2 inhibitors enables repeated administration of vaccinia virus for control of ovarian cancer. Mol. Ther. 17:81365–72
    [Google Scholar]
  16. Chen G, Luo Y, Warncke K, Sun Y, Yu DS et al. 2019. Acetylation regulates ribonucleotide reductase activity and cancer cell growth. Nat. Commun. 10:3213
    [Google Scholar]
  17. Choi UY, Lee JJ, Park A, Zhu W, Lee HR et al. 2020. Oncogenic human herpesvirus hijacks proline metabolism for tumorigenesis. PNAS 117:148083–93
    [Google Scholar]
  18. Christofk HR, Vander Heiden MG, Harris MH, Ramanathan A, Gerszten RE et al. 2008. The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth. Nature 452:230–33
    [Google Scholar]
  19. Csibi A, Lee G, Yoon SO, Tong H, Ilter D et al. 2014. The mTORC1/S6K1 pathway regulates glutamine metabolism through the eIF4B-dependent control of c-Myc translation. Curr. Biol. 24:192274–80
    [Google Scholar]
  20. Cuninghame S, Jackson R, Zehbe I 2014. Hypoxia-inducible factor 1 and its role in viral carcinogenesis. Virology 456–57 370–83
    [Google Scholar]
  21. Cunningham JT, Moreno MV, Lodi A, Ronen SM, Ruggero D 2014. Protein and nucleotide biosynthesis are coupled by a single rate-limiting enzyme, PRPS2, to drive cancer. Cell 157:51088–103
    [Google Scholar]
  22. David CJ, Chen M, Assanah M, Canoll P, Manley JL 2010. HnRNP proteins controlled by c-Myc deregulate pyruvate kinase mRNA splicing in cancer. Nature 463:364–68
    [Google Scholar]
  23. de Martel C, Ferlay J, Franceschi S, Vignat J, Bray F et al. 2012. Global burden of cancers attributable to infections in 2008: a review and synthetic analysis. Lancet Oncol 13:6607–15
    [Google Scholar]
  24. de Sanjose S, Quint WG, Alemany L, Geraets DT, Klaustermeier JE et al. 2010. Human papillomavirus genotype attribution in invasive cervical cancer: a retrospective cross-sectional worldwide study. Lancet Oncol 11:111048–56
    [Google Scholar]
  25. DeCaprio JA, Ludlow JW, Figge J, Shew JY, Huang CM et al. 1988. SV40 large tumor antigen forms a specific complex with the product of the retinoblastoma susceptibility gene. Cell 54:2275–83
    [Google Scholar]
  26. Delgado T, Carroll PA, Punjabi AS, Margineatu D, Hockenbury DM et al. 2010. Induction of the Warburg effect by Kaposi's sarcoma herpesvirus is required for the maintenance of latently infected endothelial cells. PNAS 107:2310696–701
    [Google Scholar]
  27. Delgado T, Sanchez EL, Camarda R, Lagunoff M 2012. Global metabolic profiling of infection by an oncogenic virus: KSHV induces and requires lipogenesis for survival of latent infection. PLOS Pathog 8:8e1002866
    [Google Scholar]
  28. Deng HX, Wang Y, Ding QR, Li DL, Wei YQ 2017. Gene therapy research in Asia. Gene Ther 24:9572–77
    [Google Scholar]
  29. Djeungoue-Petga M-A, Lurette O, Jean S, Hamel-Côté G, Martín-Jiménez R et al. 2020. Intramitochondrial Src kinase links mitochondrial dysfunctions and aggressiveness of breast cancer cells. Cell Death Dis 10:12940
    [Google Scholar]
  30. Dong Y, Tu R, Liu H, Qing G. 2020. Regulation of cancer cell metabolism: oncogenic MYC in the driver's seat. Signal Transduct. Target. Ther. 5:124
    [Google Scholar]
  31. Downward J, Yarden Y, Mayes E, Scrace G, Totty N et al. 1984. Close similarity of epidermal growth factor receptor and v-erb-B oncogene protein sequences. Nature 307:5951521–27
    [Google Scholar]
  32. Duesberg PH, Vogt PK. 1979. Avian acute leukemia viruses MC29 and MH2 share specific RNA sequences: evidence for a second class of transforming genes. PNAS 76:41633–37
    [Google Scholar]
  33. Duvel K, Yecies JL, Menon S, Raman P, Lipovsky AI et al. 2010. Activation of a metabolic gene regulatory network downstream of mTOR complex 1. Mol. Cell 39:2171–83
    [Google Scholar]
  34. Edmunds LR, Sharma L, Kang A, Lu J, Vockley J et al. 2014. c-Myc programs fatty acid metabolism and dictates acetyl-CoA abundance and fate. J. Biol. Chem. 289:3625382–92
    [Google Scholar]
  35. El-Serag HB, Rudolph KL 2007. Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology 132:72557–76
    [Google Scholar]
  36. Fan J, Ye J, Kamphorst JJ, Tomer S, Thompson CB et al. 2014. Quantitative flux analysis reveals folate-dependent NADPH production. Nature 510:7504298–302
    [Google Scholar]
  37. Flier JS, Mueckler MM, Usher P, Lodish HF. 1987. Elevated levels of glucose transport and transporter messenger RNA are induced by ras or src oncogenes. Science 235:47951492–95
    [Google Scholar]
  38. Fujinaga H, Tsutsumi T, Yotsuyanagi H, Moriya K, Koie K 2011. Hepatocarcinogenesis in hepatitis C: HCV shrewdly exacerbates oxidative stress by modulating both production and scavenging of reactive oxygen species. Oncology 81:111–17
    [Google Scholar]
  39. Gao P, Tchernyshyov I, Chang TC, Lee YS, Kita K et al. 2009. c-Myc suppression of miR-23a/b enhances mitochondrial glutaminase expression and glutamine metabolism. Nature 458:7239762–65
    [Google Scholar]
  40. Gao X, Sanderson SM, Dai Z, Reid MA, Cooper DE et al. 2019. Dietary methionine influences therapy in mouse cancer models and alters human metabolism. Nature 572:7769397–401
    [Google Scholar]
  41. Gouw AM, Margulis K, Liu NS, Raman SJ, Mancuso A et al. 2019. The MYC oncogene cooperates with sterol-regulated element-binding protein to regulate lipogenesis essential for neoplastic growth. Cell Metab 30:3556–72
    [Google Scholar]
  42. Gravel SP, Hulea L, Toban N, Birman E, Blouin MJ et al. 2014. Serine deprivation enhances antineoplastic activity of biguanides. Cancer Res 74:247521–33
    [Google Scholar]
  43. Guo JY, Chen HY, Mathew R, Fan J, Strohecker AM et al. 2011. Activated Ras requires autophagy to maintain oxidative metabolism and tumorigenesis. Genes Dev 25:5460–70
    [Google Scholar]
  44. Guo Y, Meng X, Ma J, Zheng Y, Wang Q et al. 2014. Human papillomavirus 16 E6 contributes HIF-1α induced Warburg effect by attenuating the VHL-HIF-1α interaction. Int. J. Mol. Sci. 15:57974–86
    [Google Scholar]
  45. Hanahan D, Weinberg RA. 2011. Hallmarks of cancer: the next generation. Cell 144:5646–74
    [Google Scholar]
  46. Hoxhaj G, Manning BD. 2019. The PI3K-AKT network at the interface of oncogenic signalling and cancer metabolism. Nat. Rev. Cancer 20:274–88
    [Google Scholar]
  47. Hu S, Balakrishnan A, Bok RA, Anderton B, Larson PEZ et al. 2011. 13C-pyruvate imaging reveals alterations in glycolysis that precede c-MYC-induced tumor formation and regression. Cell Metab 14:131–42
    [Google Scholar]
  48. Hutchison T, Malu A, Yapindi L, Bergeson R, Peck K et al. 2018. The TP53-induced glycolysis and apoptosis regulator mediates cooperation between HTLV-1 p30 II and the retroviral oncoproteins Tax and HBZ and is highly expressed in an in vivo xenograft model of HTLV-1-induced lymphoma. Virology 520:39–58
    [Google Scholar]
  49. Jin KT, Tao XH, Fan YB, Wang SB 2021. Crosstalk between oncolytic viruses and autophagy in cancer therapy. Biomed. Pharmacother. 134:110932
    [Google Scholar]
  50. Jin N, Bi A, Lan X, Xu J, Wang X et al. 2019. Identification of metabolic vulnerabilities of receptor tyrosine kinases-driven cancer. Nat. Commun. 10:2701
    [Google Scholar]
  51. Jung GS, Jeon JH, Choi YK, Jang SY, Park SY et al. 2016. Pyruvate dehydrogenase kinase regulates hepatitis C virus replication. Sci. Rep. 6:30846
    [Google Scholar]
  52. Kaiser C, Laux G, Eick D, Jochner N, Bornkamm GW et al. 1999. The proto-oncogene c-myc is a direct target gene of Epstein-Barr virus nuclear antigen 2. J. Virol. 73:54481–84
    [Google Scholar]
  53. Kaufman HL, Kohlhapp FJ, Zloza A. 2015. Oncolytic viruses: a new class of immunotherapy drugs. Nat. Rev. Drug Discov. 14:9642–62
    [Google Scholar]
  54. Khan G, Hashim MJ. 2014. Global burden of deaths from Epstein-Barr virus attributable malignancies 1990–2010. Infect. Agent. Cancer 9:38
    [Google Scholar]
  55. Killock D. 2015. T-VEC oncolytic viral therapy shows promise in melanoma. Nat. Rev. Clin. Oncol. 12:8438
    [Google Scholar]
  56. Kim JW, Zeller KI, Wang Y, Jegga AG, Aronow BJ et al. 2004. Evaluation of myc E-box phylogenetic footprints in glycolytic genes by chromatin immunoprecipitation assays. Mol. Cell. Biol. 24:135923–36
    [Google Scholar]
  57. Kodaki T, Woscholski R, Hallberg B, Rodriguez-Viciana P, Downward J et al. 1994. The activation of phosphatidylinositol 3-kinase by Ras. Curr. Biol. 4:9798–806
    [Google Scholar]
  58. Koziorowska J, Mazurowa N, Tautt J. 1990. Methionine dependence of virus-infected cells. Exp. Cell Res. 190:2290–93
    [Google Scholar]
  59. Krall AS, Mullen PJ, Surjono F, Momcilovic M, Schmid EW et al. 2021. Asparagine couples mitochondrial respiration to ATF4 activity and tumor growth. Cell Metab 33:51013–26.e6
    [Google Scholar]
  60. Krump NA, You J. 2018. Molecular mechanisms of viral oncogenesis in humans. Nat. Rev. Microbiol. 16:11684–98
    [Google Scholar]
  61. Lai MM, Hu SS, Vogt PK. 1979. Avian erythroblastosis virus: transformation-specific sequences form a contiguous segment of 3.25 kb located in the middle of the 6‑kb genome. Virology 97:2366–77
    [Google Scholar]
  62. Lane DP, Crawford LV. 1979. T antigen is bound to a host protein in SV40-transformed cells. Nature 278:5701261–63
    [Google Scholar]
  63. Lee BC, Kaya A, Ma S, Kim G, Gerashchenko MV et al. 2014. Methionine restriction extends lifespan of Drosophila melanogaster under conditions of low amino-acid status. Nat. Commun. 5:3592
    [Google Scholar]
  64. Lee P, Gujar S 2018. Potentiating prostate cancer immunotherapy with oncolytic viruses. Nat. Rev. Urol. 15:4235–50
    [Google Scholar]
  65. Leone RD, Powell JD. 2020. Metabolism of immune cells in cancer. Nat. Rev. Cancer 20:9516–31
    [Google Scholar]
  66. Levine AJ, Puzio-Kuter AM. 2010. The control of the metabolic switch in cancers by oncogenes and tumor suppressor genes. Science 330:60091340–49
    [Google Scholar]
  67. Li H, Zhu W, Zhang Lei H, Wu X et al. 2015. The metabolic responses to hepatitis B virus infection shed new light on pathogenesis and targets for treatment. Sci. Rep. 5:8421
    [Google Scholar]
  68. Liang J, Guo L, Li K, Xiao X, Zhu W et al. 2018. Inhibition of the mevalonate pathway enhances cancer cell oncolysis mediated by M1 virus. Nat. Commun. 9:1524
    [Google Scholar]
  69. Lin DC, Meng X, Hazawa M, Nagata Y, Varela AM et al. 2014. The genomic landscape of nasopharyngeal carcinoma. Nat. Genet. 46:8866–71
    [Google Scholar]
  70. Lin Y, Zhang H, Liang J, Li K, Zhu W et al. 2014. Identification and characterization of alphavirus M1 as a selective oncolytic virus targeting ZAP-defective human cancers. PNAS 111:42E4504–12
    [Google Scholar]
  71. Linzer DI, Levine AJ. 1979. Characterization of a 54K dalton cellular SV40 tumor antigen present in SV40-transformed cells and uninfected embryonal carcinoma cells. Cell 17:143–52
    [Google Scholar]
  72. Locasale JW. 2013. Serine, glycine and one-carbon units: cancer metabolism in full circle. Nat. Rev. Cancer 13:8572–83
    [Google Scholar]
  73. Lukey MJ, Greene KS, Erickson JW, Wilson KF, Cerione RA 2016. The oncogenic transcription factor c-Jun regulates glutaminase expression and sensitizes cells to glutaminase-targeted therapy. Nat. Commun. 7:11321
    [Google Scholar]
  74. Ma H, Zhang J, Zhou L, Wen S, Tang HY et al. 2020. c-Src promotes tumorigenesis and tumor progression by activating PFKFB3. Cell Rep 30:124235–49
    [Google Scholar]
  75. Ma T, Patel H, Babapoor-Farrokhran S, Franklin R, Semenza GL et al. 2015. KSHV induces aerobic glycolysis and angiogenesis through HIF-1-dependent upregulation of pyruvate kinase 2 in Kaposi's sarcoma. Angiogenesis 18:4477–88
    [Google Scholar]
  76. Maddocks ODK, Athineos D, Cheung EC, Lee P, Zhang T et al. 2017. Modulating the therapeutic response of tumours to dietary serine and glycine starvation. Nature 544:7650372–76
    [Google Scholar]
  77. Maddocks ODK, Berkers CR, Mason SM, Zheng L, Blyth K et al. 2013. Serine starvation induces stress and p53-dependent metabolic remodelling in cancer cells. Nature 493:7433542–46
    [Google Scholar]
  78. Maki Y, Bos TJ, Davis C, Starbuck M, Vogt PK. 1987. Avian sarcoma virus 17 carries the jun oncogene. PNAS 84:92848–52
    [Google Scholar]
  79. Martinez-Quintanilla J, Seah I, Chua M, Shah K. 2019. Oncolytic viruses: overcoming translational challenges. J. Clin. Investig. 129:41407–18
    [Google Scholar]
  80. McCormick F. 2005. Future prospects for oncolytic therapy. Oncogene 24:527817–19
    [Google Scholar]
  81. McFadden, Hafez AY, Kishton R, Messinger JE, Nikitin PA et al. 2016. Metabolic stress is a barrier to Epstein–Barr virus-mediated B-cell immortalization. PNAS 113:6E782–90
    [Google Scholar]
  82. Meoni G, Lorini S, Monti M, Madia F, Corti G et al. 2019. The metabolic fingerprints of HCV and HBV infections studied by nuclear magnetic resonance spectroscopy. Sci. Rep. 9:4128
    [Google Scholar]
  83. Miest TS, Cattaneo R. 2014. New viruses for cancer therapy: meeting clinical needs. Nat. Rev. Microbiol. 12:23–34
    [Google Scholar]
  84. Mohajer S, Gabliks J. 1966. The role of methionine deficiency in poliovirus replication in tissue cultures. J. Exp. Med. 123:117–24
    [Google Scholar]
  85. Moodie SA, Willumsen BM, Weber MJ, Wolfman A 1993. Complexes of Ras⋅GTP with Raf-1 and mitogen-activated protein kinase kinase. Science 260:51141658–61
    [Google Scholar]
  86. Moody CA, Scott RS, Amirghahari N, Nathan CA, Young LS et al. 2005. Modulation of the cell growth regulator mTOR by Epstein-Barr virus-encoded LMP2A. J. Virol. 79:95499–506
    [Google Scholar]
  87. Moore PS, Chang Y. 2010. Why do viruses cause cancer? Highlights of the first century of human tumour virology. Nat. Rev. Cancer 10:12878–89
    [Google Scholar]
  88. Mullen PJ, Garcia G Jr., Purkayastha A, Matulionis N, Schmid EW et al. 2021. SARS-CoV-2 infection rewires host cell metabolism and is potentially susceptible to mTORC1 inhibition. Nat. Commun. 12:1876
    [Google Scholar]
  89. Nicolay BN, Dyson NJ. 2013. The multiple connections between pRB and cell metabolism. Curr. Opin. Cell Biol. 25:6735–40
    [Google Scholar]
  90. O'Shea CC 2005a. Viruses—seeking and destroying the tumor program. Oncogene 24:527640–55
    [Google Scholar]
  91. O'Shea CC. 2005b. Viruses: tools for tumor target discovery, and agents for oncolytic therapies—an introduction. Oncogene 24:527636–39
    [Google Scholar]
  92. O'Shea CC, Klupsch K, Choi S, Bagus B, Soria C et al. 2005. Adenoviral proteins mimic nutrient/growth signals to activate the mTOR pathway for viral replication. EMBO J 24:61211–21
    [Google Scholar]
  93. Osthus RC, Shim H, Kim S, Li Q, Reddy R et al. 2000. Deregulation of glucose transporter 1 and glycolytic gene expression by c-Myc. J. Biol. Chem. 275:2921797–800
    [Google Scholar]
  94. Ou HD, Kwiatkowski W, Deerinck TJ, Noske A, Blain KY et al. 2012. A structural basis for the assembly and functions of a viral polymer that inactivates multiple tumor suppressors. Cell 151:2304–19
    [Google Scholar]
  95. Pim D, Massimi P, Dilworth SM, Banks L. 2005. Activation of the protein kinase B pathway by the HPV-16 E7 oncoprotein occurs through a mechanism involving interaction with PP2A. Oncogene 24:537830–38
    [Google Scholar]
  96. Porstmann T, Santos CR, Griffiths B, Cully M, Wu M et al. 2008. SREBP activity is regulated by mTORC1 and contributes to Akt-dependent cell growth. Cell Metab 8:3224–36
    [Google Scholar]
  97. Possemato R, Marks KM, Shaul YD, Pacold ME, Kim D et al. 2011. Functional genomics reveal that the serine synthesis pathway is essential in breast cancer. Nature 476:7360346–50
    [Google Scholar]
  98. Prior IA, Lewis PD, Mattos C. 2012. A comprehensive survey of Ras mutations in cancer. Cancer Res 72:102457–67
    [Google Scholar]
  99. Pylayeva-Gupta Y, Grabocka E, Bar-Sagi D 2011. RAS oncogenes: weaving a tumorigenic web. Nat. Rev. Cancer 11:11761–74
    [Google Scholar]
  100. Quarato G, Scrima R, Agriesti F, Moradpour D, Capitanio N et al. 2013. Targeting mitochondria in the infection strategy of the hepatitis C virus. Int. J. Biochem. Cell Biol. 45:1156–66
    [Google Scholar]
  101. Ramière C, Rodriguez J, Enache LS, Lotteau V, André P et al. 2014. Activity of hexokinase is increased by its interaction with hepatitis C virus protein NS5A. J. Virol. 88:63246–54
    [Google Scholar]
  102. Robitaille AM, Christen S, Shimobayashi M, Cornu M, Fava LL et al. 2013. Quantitative phosphoproteomics reveal mTORC1 activates de novo pyrimidine synthesis. Science 339:61251320–23
    [Google Scholar]
  103. Rodriguez-Viciana P, Warne PH, Dhand R, Vanhaesebroeck B, Gout I et al. 1994. Phosphatidylinositol-3-OH kinase as a direct target of Ras. Nature 370:6490527–32
    [Google Scholar]
  104. Roman A, Munger K. 2013. The papillomavirus E7 proteins. Virology 445:1–2138–68
    [Google Scholar]
  105. Sanderson SM, Gao X, Dai Z, Locasale JW. 2019. Methionine metabolism in health and cancer: a nexus of diet and precision medicine. Nat. Rev. Cancer 19:11625–37
    [Google Scholar]
  106. Scheffner M, Werness BA, Huibregtse A, Levine AJ, Howley PM. 1990. The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell 63:61129–36
    [Google Scholar]
  107. Schiffman M, Doorbar J, Wentzensen N, de Sanjose S, Fakhry C et al. 2016. Carcinogenic human papillomavirus infection. Nat. Rev. Dis. Primers 2:16086
    [Google Scholar]
  108. Schwarz E, Freese UK, Gissmann L, Mayer W, Roggenbuck B et al. 1985. Structure and transcription of human papillomavirus sequences in cervical carcinoma cells. Nature 314:6006111–14
    [Google Scholar]
  109. Sheiness D, Bishop JM. 1979. DNA and RNA from uninfected vertebrate cells contain nucleotide sequences related to the putative transforming gene of avian myelocytomatosis virus. J. Virol. 31:2514–21
    [Google Scholar]
  110. Sherr CJ, McCormick F. 2002. The RB and p53 pathways in cancer. Cancer Cell 2:2103–12
    [Google Scholar]
  111. Shih TY, Weeks MO, Young HA, Scholnick EM 1979. Identification of a sarcoma virus-coded phosphoprotein in nonproducer cells transformed by Kirsten or Harvey murine sarcoma virus. Virology 96:164–79
    [Google Scholar]
  112. Shim H, Dolde C, Lewis BC, Wu CS, Dang G et al. 1997. c-Myc transactivation of LDH-A: implications for tumor metabolism and growth. PNAS 4:136658–63
    [Google Scholar]
  113. Sjolander A, Yamamoto K, Huber BE, Lapetina EG. 1991. Association of p21ras with phosphatidylinositol 3-kinase. PNAS 88:187908–12
    [Google Scholar]
  114. Sommermann TG, O'Neill K, Plas DRCahir-MacFarland 2011. IKKβ and NF-κB transcription govern lymphoma cell survival through AKT-induced plasma membrane trafficking of GLUT1. Cancer Res 71:237291–300
    [Google Scholar]
  115. Spangle JM, Munger K. 2010. The human papillomavirus type 16 E6 oncoprotein activates mTORC1 signaling and increases protein synthesis. J. Virol. 84:189398–407
    [Google Scholar]
  116. Stine ZE, Walton ZE, Altman BJ, Hsieh AL, Dang CV. 2015. MYC, metabolism, and cancer. Cancer Discov 5:101024–39
    [Google Scholar]
  117. Thai M, Graham NA, Braas D, Nehil M, Komisopoulou E et al. 2014. Adenovirus E4ORF1-induced MYC activation promotes host cell anabolic glucose metabolism and virus replication. Cell Metab 19:4694–701
    [Google Scholar]
  118. Thai M, Thaker SK, Feng J, Du Y, Hu H et al. 2015. MYC-induced reprogramming of glutamine catabolism supports optimal virus replication. Nat. Commun. 6:8873
    [Google Scholar]
  119. Thaker SK, Ch'ng J, Christofk HR. 2019. Viral hijacking of cellular metabolism. BMC Biol 17:59
    [Google Scholar]
  120. Thomas MA, Broughton RS, Goodrum FD, Ornelles DA. 2009. E4orf1 limits the oncolytic potential of the E1B-55K deletion mutant adenovirus. J. Virol. 83:62406–16
    [Google Scholar]
  121. Tsuchida N, Ryder T, Ohtsubo E. 1982. Nucleotide sequence of the oncogene encoding the p21 transforming protein of Kirsten murine sarcoma virus. Science 217:4563937–39
    [Google Scholar]
  122. Tu WB, Helander S, Pilstal R, Hickman KA, Lourenco C et al. 2015. Myc and its interactors take shape. Biochim. Biophys. Acta 1849:5469–83
    [Google Scholar]
  123. Ullrich A, Coussens L, Hayflick JS, Dull TJ, Gray A et al. 1984. Human epidermal growth factor receptor cDNA sequence and aberrant expression of the amplified gene in A431 epidermoid carcinoma cells. Nature 309:5967418–25
    [Google Scholar]
  124. Valvezan AJ, Manning BD. 2019. Molecular logic of mTORC1 signalling as a metabolic rheostat. Nat. Metab. 1:3321–33
    [Google Scholar]
  125. Vande Pol SB, Klingelhutz AJ 2013. Papillomavirus E6 oncoproteins. Virology 445:1–2115–37
    [Google Scholar]
  126. Venkateswaren N, Lafita-Navarro MC, Hao YH, Kilgore JA, Perez-Castro L et al. 2019. MYC promotes tryptophan uptake and metabolism by the kynurenine pathway in colon cancer. Genes Dev 33:17–181236–51
    [Google Scholar]
  127. Vogt PK. 2001. Jun, the oncoprotein. Oncogene 20:19265–77
    [Google Scholar]
  128. Vojtek AB, Hollenberg SM, Cooper JA. 1993. Mammalian Ras interacts directly with the serine/threonine kinase Raf. Cell 74:1205–14
    [Google Scholar]
  129. Vousden KH, Ryan KM. 2009. p53 and metabolism. Nat. Rev. Cancer 9:10691–700
    [Google Scholar]
  130. Wang LW, Shen H, Nobre L, Ersing I, Paulo JA et al. 2019. Epstein-Barr-virus-induced one-carbon metabolism drives B cell transformation. Cell Metab 30:3539–555
    [Google Scholar]
  131. Wang X, Yang K, Xie Q, Wu Q, Mack SC et al. 2017. Purine synthesis promotes maintenance of brain tumor initiating cells in glioma. Nat. Neurosci. 20:5661–73
    [Google Scholar]
  132. White E. 2013. Exploiting the bad eating habits of Ras-driven cancers. Genes Dev 27:192065–71
    [Google Scholar]
  133. Whitman M, Kaplan DR, Schaffhausen B, Cantley L, Roberts TM 1985. Association of phosphatidylinositol kinase activity with polyoma middle-T competent for transformation. Nature 315:6016239–42
    [Google Scholar]
  134. Whyte P, Buchkovich KJ, Horowitz JM, Friend SH, Raybuck M et al. 1988. Association between an oncogene and an anti-oncogene: the adenovirus E1A proteins bind to the retinoblastoma gene product. Nature 334:6178124–29
    [Google Scholar]
  135. Wise DR, DeBerardinis RJ, Mancuso A, Sayed N, Zhang XY et al. 2008. Myc regulates a transcriptional program that stimulates mitochondrial glutaminolysis and leads to glutamine addiction. PNAS 105:4818782–87
    [Google Scholar]
  136. Wolf E, Eilers M 2020. Targeting MYC proteins for tumor therapy. Annu. Rev. Cancer Biol. 4:61–75
    [Google Scholar]
  137. Wood KW, Sarnecki C, Roberts TM, Blenis J. 1992. ras mediates nerve growth factor receptor modulation of three signal-transducing protein kinases: MAP kinase, Raf-1, and RSK. Cell 68:61041–50
    [Google Scholar]
  138. Xiao L, Hu ZY, Dong X, Tan Z, Li W et al. 2014. Targeting Epstein-Barr virus oncoprotein LMP1-mediated glycolysis sensitizes nasopharyngeal carcinoma to radiation therapy. Oncogene 33:374568–78
    [Google Scholar]
  139. Xie Q, Fan F, Wei W, Liu Y, Xu Z et al. 2017. Multi-omics analyses reveal metabolic alterations regulated by hepatitis B virus core protein in hepatocellular carcinoma cells. Sci. Rep. 7:41089
    [Google Scholar]
  140. Yang S, Wang X, Contino G, Liesa M, Sahin E et al. 2011. Pancreatic cancers require autophagy for tumor growth. Genes Dev 25:7717–29
    [Google Scholar]
  141. Young LS, Yap LF, Murray PG. 2016. Epstein-Barr virus: more than 50 years old and still providing surprises. Nat. Rev. Cancer 16:12789–802
    [Google Scholar]
  142. Yue D, Zhang Y, Cheng L, Ma J, Xi Y et al. 2016. Hepatitis B virus X protein (HBx)-induced abnormalities of nucleic acid metabolism revealed by 1H-NMR-based metabonomics. Sci. Rep. 6:24430
    [Google Scholar]
  143. Yue M, Jiang J, Gao P, Liu H, Qing G. 2017. Oncogenic MYC activates a feedforward regulatory loop promoting essential amino acid metabolism and tumorigenesis. Cell Rep 21:133819–32
    [Google Scholar]
  144. Zelenay S, van der Veen AG, Bottcher JP, Snelgrove J, Rogers N et al. 2015. Cyclooxygenase-dependent tumor growth through evasion of immunity. Cell 162:61257–70
    [Google Scholar]
  145. Zhang J, Wang S, Jiang B, Huang L, Ji Z et al. 2017. c-Src phosphorylation and activation of hexokinase promotes tumorigenesis and metastasis. Nat. Commun. 8:13732
    [Google Scholar]
  146. Zhang Y, Guo R, Kim SH, Shah H, Zhang S et al. 2021. SARS-CoV-2 hijacks folate and one-carbon metabolism for viral replication. Nat. Commun. 12:1676
    [Google Scholar]
  147. Zheng L, Ding H, Lu Z, Li Y, Pan Y et al. 2008. E3 ubiquitin ligase E6AP-mediated TSC2 turnover in the presence and absence of HPV16 E6. Genes Cells 13:3285–94
    [Google Scholar]
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