Metabolic reprogramming: A hallmark of viral oncogenesis

Oncogene

Volumn 35, Issue 32, 2016, Pages 4155-4164

  Levy P ^a   Bartosch, B ^a,b  

^a CENTRE DE RECHERCHE EN CANCÉROLOGIE DE LYON   (France)

^b DevWeCan Laboratories of Excellence Network (Labex)   (France)

Author keywords

[No Author keywords available]

Indexed keywords

TUMOR SUPPRESSOR PROTEIN;

ADENOVIRIDAE; ANTINEOPLASTIC ACTIVITY; BIOSYNTHESIS; CELL CYCLE PROGRESSION; CELL DEATH; CELL METABOLISM; CELL TRANSFORMATION; EPSTEIN BARR VIRUS; HEPATITIS B VIRUS; HEPATITIS C VIRUS; HERPESVIRIDAE; HUMAN; HUMAN CYTOMEGALOVIRUS; HUMAN T-LYMPHOTROPIC VIRUS 1; METABOLIC REGULATION; NONHUMAN; NUCLEAR REPROGRAMMING; ONCOGENE; PRIORITY JOURNAL; REVIEW; TUMOR VIRUS; VIRUS CARCINOGENESIS; VIRUS CELL INTERACTION; VIRUS REPLICATION; WART VIRUS; ANIMAL; CARCINOGENESIS; GENETICS; METABOLISM; NEOPLASM; PATHOLOGY; VIRAL PHENOMENA AND FUNCTIONS; VIROLOGY;

ANIMALS; CARCINOGENESIS; HUMANS; NEOPLASMS; VIRUS PHYSIOLOGICAL PHENOMENA;

EID: 84951325596     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2015.479     Document Type: Review

References (177)

1. de Martel C, Ferlay J, Franceschi S, Vignat J, Bray F, Forman D et al. Global burden of cancers attributable to infections in 2008: a review and synthetic analysis. Lancet Oncol 2012; 13: 607-615.
2. Mesri EA, Feitelson MA, Munger K. Human viral oncogenesis: a cancer hallmarks analysis. Cell Host Microbe 2014; 15: 266-282.
3. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell 2000; 100: 57-70.
4. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011; 144: 646-674.
5. Koppenol WH, Bounds PL, Dang CV. Otto Warburg's contributions to current concepts of cancer metabolism. Nat Rev Cancer 2011; 11: 325-337.
6. Ward PS, Thompson CB. Metabolic reprogramming: a cancer hallmark even warburg did not anticipate. Cancer Cell 2012; 21: 297-308.
7. Racker E. Bioenergetics and the problem of tumor growth. Am Sci 1972; 60: 56-63.
8. Weinhouse S. On respiratory impairment in cancer cells. Science 1956; 124: 267.
9. Zu XL, Guppy M. Cancer metabolism: facts, fantasy, and fiction. Biochem Biophys Res Commun 2004; 313: 459-465.
10. Moreno-Sanchez R, Rodriguez-Enriquez S, Marin-Hernandez A, Saavedra E. Energy metabolism in tumor cells. FEBS J 2007; 274: 1393-1418.
11. Fantin VR, St-Pierre J, Leder P. Attenuation of LDH-A expression uncovers a link between glycolysis, mitochondrial physiology, and tumor maintenance. Cancer Cell 2006; 9: 425-434.
12. Fan J, Kamphorst JJ, Mathew R, Chung MK, White E, Shlomi T et al. Glutaminedriven oxidative phosphorylation is a major ATP source in transformed mammalian cells in both normoxia and hypoxia. Mol Syst Biol 2013; 9: 712.
13. Lunt SY, Vander Heiden MG. Aerobic glycolysis: meeting the metabolic requirements of cell proliferation. Annu Rev Cell Dev Biol 2011; 27: 441-464.
14. Medes G, Thomas A, Weinhouse S. Metabolism of neoplastic tissue. IV. A study of lipid synthesis in neoplastic tissue slices in vitro. Cancer Res 1953; 13: 27-29.
15. Menendez JA, Lupu R. Fatty acid synthase and the lipogenic phenotype in cancer pathogenesis. Nat Rev Cancer 2007; 7: 763-777.
16. DeBerardinis RJ, Lum JJ, Hatzivassiliou G, Thompson CB. The biology of cancer: metabolic reprogramming fuels cell growth and proliferation. Cell Metab 2008; 7: 11-20.
17. DeBerardinis RJ, Cheng T. Q's next: the diverse functions of glutamine in metabolism, cell biology and cancer. Oncogene 2010; 29: 313-324.
18. Shaw RJ, Cantley LC. Ras, PI(3)K and mTOR signalling controls tumour cell growth. Nature 2006; 441: 424-430.
19. Vanhaesebroeck B, Stephens L, Hawkins P. PI3K signalling: the path to discovery and understanding. Nat Rev Mol Cell Biol 2012; 13: 195-203.
20. Bauer DE, Hatzivassiliou G, Zhao F, Andreadis C, Thompson CB. ATP citrate lyase is an important component of cell growth and transformation. Oncogene 2005; 24: 6314-6322.
21. Laplante M, Sabatini DM. mTOR signaling in growth control and disease. Cell 2012; 149: 274-293.
22. Peterson TR, Sengupta SS, Harris TE, Carmack AE, Kang SA, Balderas E et al. mTOR complex 1 regulates lipin 1 localization to control the SREBP pathway. Cell 2011; 146: 408-420.
23. Duvel K, Yecies JL, Menon S, Raman P, Lipovsky AI, Souza AL et al. Activation of a metabolic gene regulatory network downstream of mTOR complex 1. Mol Cell 2010; 39: 171-183.
24. Kim JE, Chen J. regulation of peroxisome proliferator-activated receptor-gamma activity by mammalian target of rapamycin and amino acids in adipogenesis. Diabetes 2004; 53: 2748-2756.
25. Ben-Sahra I, Howell JJ, Asara JM, Manning BD. Stimulation of de novo pyrimidine synthesis by growth signaling through mTOR and S6K1. Science 2013; 339: 1323-1328.
26. Keith B, Johnson RS, Simon MC. HIF1alpha and HIF2alpha: sibling rivalry in hypoxic tumour growth and progression. Nat Rev Cancer 2012; 12: 9-22.
27. Schodel J, Oikonomopoulos S, Ragoussis J, Pugh CW, Ratcliffe PJ, Mole DR. Highresolution genome-wide mapping of HIF-binding sites by ChIP-seq. Blood 2011; 117: e207-e217.
28. Papandreou I, Cairns RA, Fontana L, Lim AL, Denko NC. HIF-1 mediates adaptation to hypoxia by actively downregulating mitochondrial oxygen consumption. Cell Metab 2006; 3: 187-197.
29. Firth JD, Ebert BL, Pugh CW, Ratcliffe PJ. Oxygen-regulated control elements in the phosphoglycerate kinase 1 and lactate dehydrogenase A genes: similarities with the erythropoietin 3' enhancer. Proc Natl Acad Sci USA 1994; 91: 6496-6500.
30. Metallo CM, Gameiro PA, Bell EL, Mattaini KR, Yang J, Hiller K et al. Reductive glutamine metabolism by IDH1 mediates lipogenesis under hypoxia. Nature 2012; 481: 380-384.
31. Wise DR, Ward PS, Shay JE, Cross JR, Gruber JJ, Sachdeva UM et al. Hypoxia promotes isocitrate dehydrogenase-dependent carboxylation of alphaketoglutarate to citrate to support cell growth and viability. Proc Natl Acad Sci USA 2011; 108: 19611-19616.
32. Gameiro PA, Yang J, Metelo AM, Perez-Carro R, Baker R, Wang Z et al. In vivo HIFmediated reductive carboxylation is regulated by citrate levels and sensitizes VHL-deficient cells to glutamine deprivation. Cell Metab 2013; 17: 372-385.
33. Pylayeva-Gupta Y, Grabocka E, Bar-Sagi D. RAS oncogenes: weaving a tumorigenic web. Nat Rev Cancer 2011; 11: 761-774.
34. Ying H, Kimmelman AC, Lyssiotis CA, Hua S, Chu GC, Fletcher-Sananikone E et al. Oncogenic Kras maintains pancreatic tumors through regulation of anabolic glucose metabolism. Cell 2012; 149: 656-670.
35. Kikuchi H, Pino MS, Zeng M, Shirasawa S, Chung DC. Oncogenic KRAS and BRAF differentially regulate hypoxia-inducible factor-1alpha and -2alpha in colon cancer. Cancer Res 2009; 69: 8499-8506.
36. Commisso C, Davidson SM, Soydaner-Azeloglu RG, Parker SJ, Kamphorst JJ, Hackett S et al. Macropinocytosis of protein is an amino acid supply route in Rastransformed cells. Nature 2013; 497: 633-637.
37. Son J, Lyssiotis CA, Ying H, Wang X, Hua S, Ligorio M et al. Glutamine supports pancreatic cancer growth through a KRAS-regulated metabolic pathway. Nature 2013; 496: 101-105.
38. Vogt PK. Retroviral oncogenes: a historical primer. Nat Rev Cancer 2012; 12: 639-648.
39. Wierstra I, Alves J. The c-myc promoter: still MysterY and challenge. Adv Cancer Res 2008; 99: 113-333.
40. Osthus RC, Shim H, Kim S, Li Q, Reddy R, Mukherjee M et al. Deregulation of glucose transporter 1 and glycolytic gene expression by c-Myc. J Biol Chem 2000; 275: 21797-21800.
41. Kim JW, Zeller KI, Wang Y, Jegga AG, Aronow BJ, O'Donnell KA et al. Evaluation of myc E-box phylogenetic footprints in glycolytic genes by chromatin immunoprecipitation assays. Mol Cell Biol 2004; 24: 5923-5936.
42. David CJ, Chen M, Assanah M, Canoll P, Manley JL. HnRNP proteins controlled by c-Myc deregulate pyruvate kinase mRNA splicing in cancer. Nature 2010; 463: 364-368.
43. Amelio I, Cutruzzola F, Antonov A, Agostini M, Melino G. Serine and glycine metabolism in cancer. Trends Biochem Sci 2014; 39: 191-198.
44. Vazquez A, Tedeschi PM, Bertino JR. Overexpression of the mitochondrial folate and glycine-serine pathway: a new determinant of methotrexate selectivity in tumors. Cancer Res 2013; 73: 478-482.
45. Morrish F, Hockenbery D. MYC and mitochondrial biogenesis. Cold Spring Harb Perspect Med 2014; 4: 5.
46. Yuneva M, Zamboni N, Oefner P, Sachidanandam R, Lazebnik Y. Deficiency in glutamine but not glucose induces MYC-dependent apoptosis in human cells. J Cell Biol 2007; 178: 93-105.
47. Wise DR, DeBerardinis RJ, Mancuso A, Sayed N, Zhang XY, Pfeiffer HK et al. Myc regulates a transcriptional program that stimulates mitochondrial glutaminolysis and leads to glutamine addiction. Proc Natl Acad Sci USA 2008; 105: 18782-18787.
48. Le A, Lane AN, Hamaker M, Bose S, Gouw A, Barbi J et al. Glucose-independent glutamine metabolism via TCA cycling for proliferation and survival in B cells. Cell Metab 2012; 15: 110-121.
49. Wang R, Dillon CP, Shi LZ, Milasta S, Carter R, Finkelstein D et al. The transcription factor Myc controls metabolic reprogramming upon T lymphocyte activation. Immunity 2011; 35: 871-882.
50. Bieging KT, Mello SS, Attardi LD. Unravelling mechanisms of p53-mediated tumour suppression. Nat Rev Cancer 2014; 14: 359-370.
51. Berkers CR, Maddocks OD, Cheung EC, Mor I, Vousden KH. Metabolic regulation by p53 family members. Cell Metab 2013; 18: 617-633.
52. Vousden KH, Ryan KM. p53 and metabolism. Nat Rev Cancer 2009; 9: 691-700.
53. Song MS, Salmena L, Pandolfi PP. The functions and regulation of the PTEN tumour suppressor. Nat Rev Mol Cell Biol 2012; 13: 283-296.
54. Garcia-Cao I, Song MS, Hobbs RM, Laurent G, Giorgi C, de Boer VC et al. Systemic elevation of PTEN induces a tumor-suppressive metabolic state. Cell 2012; 149: 49-62.
55. Shackelford DB, Shaw RJ. The LKB1-AMPK pathway: metabolism and growth control in tumour suppression. Nat Rev Cancer 2009; 9: 563-575.
56. Li Y, Xu S, Mihaylova MM, Zheng B, Hou X, Jiang B et al. AMPK phosphorylates and inhibits SREBP activity to attenuate hepatic steatosis and atherosclerosis in diet-induced insulin-resistant mice. Cell Metab 2011; 13: 376-388.
57. Faubert B, Boily G, Izreig S, Griss T, Samborska B, Dong Z et al. AMPK is a negative regulator of the Warburg effect and suppresses tumor growth in vivo. Cell Metab 2013; 17: 113-124.
58. Treins C, Murdaca J, Van Obberghen E, Giorgetti-Peraldi S. AMPK activation inhibits the expression of HIF-1alpha induced by insulin and IGF-1. Biochem Biophys Res Commun 2006; 342: 1197-1202.
59. Knudsen ES, Knudsen KE. Tailoring to RB: tumour suppressor status and therapeutic response. Nat Rev Cancer 2008; 8: 714-724.
60. Angus SP, Wheeler LJ, Ranmal SA, Zhang X, Markey MP, Mathews CK et al. Retinoblastoma tumor suppressor targets dNTP metabolism to regulate DNA replication. J Biol Chem 2002; 277: 44376-44384.
61. Nicolay BN, Dyson NJ. The multiple connections between pRB and cell metabolism. Curr Opin Cell Biol 2013; 25: 735-740.
62. Fajas L. Re-thinking cell cycle regulators: the cross-talk with metabolism. Front Oncol 2013; 3: 4.
63. Blanchet E, Annicotte JS, Lagarrigue S, Aguilar V, Clape C, Chavey C et al. E2F transcription factor-1 regulates oxidative metabolism. Nat Cell Biol 2011; 13: 1146-1152.
64. Claus C, Liebert UG. A renewed focus on the interplay between viruses and mitochondrial metabolism. Arch Virol 2014; 159: 1267-1277.
65. El-Bacha T, Da Poian AT. Virus-induced changes in mitochondrial bioenergetics as potential targets for therapy. Int J Biochem Cell Biol 2013; 45: 41-46.
66. Crosbie EJ, Einstein MH, Franceschi S, Kitchener HC. Human papillomavirus and cervical cancer. Lancet 2013; 382: 889-899.
67. Longworth MS, Laimins LA. Pathogenesis of human papillomaviruses in differentiating epithelia. Microbiol Mol Biol Rev 2004; 68: 362-372.
68. Tommasino M, Accardi R, Caldeira S, Dong W, Malanchi I, Smet A et al. The role of TP53 in Cervical carcinogenesis. Hum Mutat 2003; 21: 307-312.
69. Munger K, Basile JR, Duensing S, Eichten A, Gonzalez SL, Grace M et al. Biological activities and molecular targets of the human papillomavirus E7 oncoprotein. Oncogene 2001; 20: 7888-7898.
70. Zwerschke W, Mazurek S, Massimi P, Banks L, Eigenbrodt E, Jansen-Durr P. Modulation of type M2 pyruvate kinase activity by the human papillomavirus type 16 E7 oncoprotein. Proc Natl Acad Sci USA 1999; 96: 1291-1296.
71. Mazurek S. Pyruvate kinase type M2: a key regulator of the metabolic budget system in tumor cells. Int J Biochem Cell Biol 2011; 43: 969-980.
72. Mazurek S, Zwerschke W, Jansen-Durr P, Eigenbrodt E. Metabolic cooperation between different oncogenes during cell transformation: interaction between activated ras and HPV-16 E7. Oncogene 2001; 20: 6891-6898.
73. Mazurek S, Zwerschke W, Jansen-Durr P, Eigenbrodt E. Effects of the human papilloma virus HPV-16 E7 oncoprotein on glycolysis and glutaminolysis: role of pyruvate kinase type M2 and the glycolytic-enzyme complex. Biochem J 2001; 356: 247-256.
74. Spangle JM, Munger K. The human papillomavirus type 16 E6 oncoprotein activates mTORC1 signaling and increases protein synthesis. J Virol 2010; 84: 9398-9407.
75. Pim D, Massimi P, Dilworth SM, Banks L. Activation of the protein kinase B pathway by the HPV-16 E7 oncoprotein occurs through a mechanism involving interaction with PP2A. Oncogene 2005; 24: 7830-7838.
76. Tang X, Zhang Q, Nishitani J, Brown J, Shi S, Le AD. Overexpression of human papillomavirus type 16 oncoproteins enhances hypoxia-inducible factor 1 alpha protein accumulation and vascular endothelial growth factor expression in human cervical carcinoma cells. Clin Cancer Res 2007; 13: 2568-2576.
77. Bodily JM, Mehta KP, Laimins LA. Human papillomavirus E7 enhances hypoxiainducible factor 1-mediated transcription by inhibiting binding of histone deacetylases. Cancer Res 2011; 71: 1187-1195.
78. Maehama T, Patzelt A, Lengert M, Hutter KJ, Kanazawa K, Hausen H et al. Selective down-regulation of human papillomavirus transcription by 2- deoxyglucose. Int J Cancer 1998; 76: 639-646.
79. Molinolo AA, Marsh C, El Dinali M, Gangane N, Jennison K, Hewitt S et al. mTOR as a molecular target in HPV-associated oral and cervical squamous carcinomas. Clin Cancer Res 2012; 18: 2558-2568.
80. Henken FE, Banerjee NS, Snijders PJ, Meijer CJ, De-Castro Arce J, Rosl F et al. PIK3CA-mediated PI3-kinase signalling is essential for HPV-induced transformation in vitro. Mol Cancer 2011; 10: 71.
81. Poiesz BJ, Ruscetti FW, Gazdar AF, Bunn PA, Minna JD, Gallo RC. Detection and isolation of type C retrovirus particles from fresh and cultured lymphocytes of a patient with cutaneous T-cell lymphoma. Proc Natl Acad Sci USA 1980; 77: 7415-7419.
82. Gessain A, Cassar O. Epidemiological aspects and world distribution of HTLV-1 infection. Front Microbiol 2012; 3: 388.
83. Proietti FA, Carneiro-Proietti AB, Catalan-Soares BC, Murphy EL. Global epidemiology of HTLV-I infection and associated diseases. Oncogene 2005; 24: 6058-6068.
84. Matsuoka M, Jeang KT. Human T-cell leukemia virus type 1 (HTLV-1) and leukemic transformation: viral infectivity, Tax, HBZ and therapy. Oncogene 2011; 30: 1379-1389.
85. Mukai R, Ohshima T. HTLV-1 HBZ positively regulates the mTOR signaling pathway via inhibition of GADD34 activity in the cytoplasm. Oncogene 2014; 33: 2317-2328.
86. Manel N, Kim FJ, Kinet S, Taylor N, Sitbon M, Battini JL. The ubiquitous glucose transporter GLUT-1 is a receptor for HTLV. Cell 2003; 115: 449-459.
87. Sripadi P, Shrestha B, Easley RL, Carpio L, Kehn-Hall K, Chevalier S et al. Direct detection of diverse metabolic changes in virally transformed and tax-expressing cells by mass spectrometry. PLoS One 2010; 5: e12590.
88. Straus S. Adenovirus infections in humans. In: Ginsberg H (ed). The Adenoviruses. Springer: New York, NY, USA, 1984, pp 451-496.
89. Lenaerts L, De Clercq E, Naesens L. Clinical features and treatment of adenovirus infections. Rev Med Virol 2008; 18: 357-374.
90. Graham FL. Transformation by and oncogenicity of human adenoviruses. In: Ginsberg H (ed). The Adenoviruses. Springer: New York, NY, USA, 1984, pp 339-398.
91. Berk AJ. Recent lessons in gene expression, cell cycle control, and cell biology from adenovirus. Oncogene 2005; 24: 7673-7685.
92. Thai M, Graham NA, Braas D, Nehil M, Komisopoulou E, Kurdistani SK et al. Adenovirus E4ORF1-induced MYC activation promotes host cell anabolic glucose metabolism and virus replication. Cell Metab 2014; 19: 694-701.
93. O'Shea C, Klupsch K, Choi S, Bagus B, Soria C, Shen J et al. Adenoviral proteins mimic nutrient/growth signals to activate the mTOR pathway for viral replication. EMBO J 2005; 24: 1211-1221.
94. Frese KK, Lee SS, Thomas DL, Latorre IJ, Weiss RS, Glaunsinger BA et al. Selective PDZ protein-dependent stimulation of phosphatidylinositol 3-kinase by the adenovirus E4-ORF1 oncoprotein. Oncogene 2003; 22: 710-721.
95. Kong K, Kumar M, Taruishi M, Javier RT. The human adenovirus E4-ORF1 protein subverts discs large 1 to mediate membrane recruitment and dysregulation of phosphatidylinositol 3-kinase. PLoS Pathog 2014; 10: e1004102.
96. Rogers PM, Mashtalir N, Rathod MA, Dubuisson O, Wang Z, Dasuri K et al. Metabolically favorable remodeling of human adipose tissue by human adenovirus type 36. Diabetes 2008; 57: 2321-2331.
97. Wang ZQ, Yu Y, Zhang XH, Floyd EZ, Cefalu WT. Human adenovirus 36 decreases fatty acid oxidation and increases de novo lipogenesis in primary cultured human skeletal muscle cells by promoting Cidec/FSP27 expression. Int J Obes (Lond) 2010; 34: 1355-1364.
98. El-Serag HB. Epidemiology of viral hepatitis and hepatocellular carcinoma. Gastroenterology 2012; 142: 1264-1273 e1.
99. El-Serag HB, Rudolph KL. Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology 2007; 132: 2557-2576.
100. Arzumanyan A, Reis HM, Feitelson MA. Pathogenic mechanisms in HBVand HCV-associated hepatocellular carcinoma. Nat Rev Cancer 2013; 13: 123-135.
101. Lemon SM, McGivern DR. Is hepatitis C virus carcinogenic? Gastroenterology 2012; 142: 1274-1278.
102. Li H, Zhu W, Zhang L, Lei H, Wu X, Guo L et al. The metabolic responses to hepatitis B virus infection shed new light on pathogenesis and targets for treatment. Sci Rep 2015; 5: 8421.
103. Teng CF, Hsieh WC, Wu HC, Lin YJ, Tsai HW, Huang W et al. Hepatitis B virus pre- S2 mutant induces aerobic glycolysis through mammalian target of rapamycin signal cascade. PLoS One 2015; 10: e0122373.
104. Teng CF, Wu HC, Hsieh WC, Tsai HW, Su IJ. Activation of ATP citrate lyase by mTOR signal induces disturbed lipid metabolism in hepatitis B virus pre-S2 mutant tumorigenesis. J Virol 2015; 89: 605-614.
105. Na TY, Shin YK, Roh KJ, Kang SA, Hong I, Oh SJ et al. Liver X receptor mediates hepatitis B virus X protein-induced lipogenesis in hepatitis B virus-associated hepatocellular carcinoma. Hepatology 2009; 49: 1122-1131.
106. You X, Liu F, Zhang T, Li Y, Ye L, Zhang X. Hepatitis B virus X protein upregulates oncogene Rab18 to result in the dysregulation of lipogenesis and proliferation of hepatoma cells. Carcinogenesis 2013; 34: 1644-1652.
107. Bard-Chapeau EA, Nguyen AT, Rust AG, Sayadi A, Lee P, Chua BQ et al. Transposon mutagenesis identifies genes driving hepatocellular carcinoma in a chronic hepatitis B mouse model. Nat Genet 2014; 46: 24-32.
108. Bugianesi E, Salamone F, Negro F. The interaction of metabolic factors with HCV infection: does it matter? J Hepatol 2012; 56: S56-S65.
109. Li Q, Pene V, Krishnamurthy S, Cha H, Liang TJ. Hepatitis C virus infection activates an innate pathway involving IKK-alpha in lipogenesis and viral assembly. Nat Med 2013; 19: 722-729.
110. Amako Y, Munakata T, Kohara M, Siddiqui A, Peers C, Harris M. Hepatitis C virus attenuates mitochondrial lipid beta-oxidation by downregulating mitochondrial trifunctional-protein expression. J Virol 2015; 89: 4092-4101.
111. Negro F. Abnormalities of lipid metabolism in hepatitis C virus infection. Gut 2010; 59: 1279-1287.
112. Negro F. Facts and fictions of HCV and comorbidities: steatosis, diabetes mellitus, and cardiovascular diseases. J Hepatol 2014; 61: S69-S78.
113. Ripoli M, D'Aprile A, Quarato G, Sarasin-Filipowicz M, Gouttenoire J, Scrima R et al. Hepatitis C virus-linked mitochondrial dysfunction promotes hypoxiainducible factor 1 alpha-mediated glycolytic adaptation. J Virol 2010; 84: 647-660.
114. Nasimuzzaman M, Waris G, Mikolon D, Stupack DG, Siddiqui A. Hepatitis C virus stabilizes hypoxia-inducible factor 1alpha and stimulates the synthesis of vascular endothelial growth factor. J Virol 2007; 81: 10249-10257.
115. Ramiere C, Rodriguez J, Enache LS, Lotteau V, Andre P, Diaz O. Activity of hexokinase is increased by its interaction with hepatitis C virus protein NS5A. J Virol 2014; 88: 3246-3254.
116. Wu X, Zhou Y, Zhang K, Liu Q, Guo D. Isoform-specific interaction of pyruvate kinase with hepatitis C virus NS5B. FEBS Lett 2008; 582: 2155-2160.
117. Diamond DL, Syder AJ, Jacobs JM, Sorensen CM, Walters KA, Proll SC et al. Temporal proteome and lipidome profiles reveal hepatitis C virus-associated reprogramming of hepatocellular metabolism and bioenergetics. PLoS Pathog 2010; 6: e1000719.
118. Young LS, Rickinson AB. Epstein-Barr virus: 40 years on. Nat Rev Cancer 2004; 4: 757-768.
119. Taylor GS, Blackbourn DJ. Infectious agents in human cancers: lessons in immunity and immunomodulation from gammaherpesviruses EBV and KSHV. Cancer Lett 2011; 305: 263-278.
120. Kaiser C, Laux G, Eick D, Jochner N, Bornkamm GW, Kempkes B. The protooncogene c-myc is a direct target gene of Epstein-Barr virus nuclear antigen 2. J Virol 1999; 73: 4481-4484.
121. Dawson CW, Port RJ, Young LS. The role of the EBV-encoded latent membrane proteins LMP1 and LMP2 in the pathogenesis of nasopharyngeal carcinoma (NPC). Semin Cancer Biol 2012; 22: 144-153.
122. Darekar S, Georgiou K, Yurchenko M, Yenamandra SP, Chachami G, Simos G et al. Epstein-Barr virus immortalization of human B-cells leads to stabilization of hypoxia-induced factor 1 alpha, congruent with the Warburg effect. PLoS One 2012; 7: e42072.
123. Xiao L, Hu ZY, Dong X, Tan Z, Li W, Tang M et al. Targeting Epstein-Barr virus oncoprotein LMP1-mediated glycolysis sensitizes nasopharyngeal carcinoma to radiation therapy. Oncogene 2014; 33: 4568-4578.
124. Ganem D. KSHV and the pathogenesis of Kaposi sarcoma: listening to human biology and medicine. J Clin Invest 2010; 120: 939-949.
125. Uldrick TS, Whitby D. Update on KSHV epidemiology, Kaposi Sarcoma pathogenesis, and treatment of Kaposi Sarcoma. Cancer Lett 2011; 305: 150-162.
126. Jones JL, Hanson DL, Dworkin MS, Ward JW, Jaffe HW. Effect of antiretroviral therapy on recent trends in selected cancers among HIV-infected persons. Adult/ Adolescent Spectrum of HIV Disease Project Group. J Acquir Immune Defic Syndr 1999; 21: S11-S17.
127. Mesri EA, Cesarman E, Boshoff C. Kaposi's sarcoma and its associated herpesvirus. Nat Rev Cancer 2010; 10: 707-719.
128. Friborg Jr J, Kong W, Hottiger MO, Nabel GJ. p53 inhibition by the LANA protein of KSHV protects against cell death. Nature 1999; 402: 889-894.
129. Radkov SA, Kellam P, Boshoff C. The latent nuclear antigen of Kaposi sarcoma-associated herpesvirus targets the retinoblastoma-E2F pathway and with the oncogene Hras transforms primary rat cells. Nat Med 2000; 6: 1121-1127.
130. Cai QL, Knight JS, Verma SC, Zald P, Robertson ES. EC5S ubiquitin complex is recruited by KSHV latent antigen LANA for degradation of the VHL and p53 tumor suppressors. PLoS Pathog 2006; 2: e116.
131. Shin YC, Joo CH, Gack MU, Lee HR, Jung JU. Kaposi's sarcoma-associated herpesvirus viral IFN regulatory factor 3 stabilizes hypoxia-inducible factor-1 alpha to induce vascular endothelial growth factor expression. Cancer Res 2008; 68: 1751-1759.
132. Carroll PA, Kenerson HL, Yeung RS, Lagunoff M. Latent Kaposi's sarcomaassociated herpesvirus infection of endothelial cells activates hypoxia-induced factors. J Virol 2006; 80: 10802-10812.
133. Cai Q, Murakami M, Si H, Robertson ES. A potential alpha-helix motif in the amino terminus of LANA encoded by Kaposi's sarcoma-associated herpesvirus is critical for nuclear accumulation of HIF-1alpha in normoxia. J Virol 2007; 81: 10413-10423.
134. Cavallin LE, Goldschmidt-Clermont P, Mesri EA. Molecular and cellular mechanisms of KSHV oncogenesis of Kaposi's sarcoma associated with HIV/AIDS. PLoS Pathog 2014; 10: e1004154.
135. Bhatt AP, Damania B. AKTivation of PI3K/AKT/mTOR signaling pathway by KSHV. Front Immunol 2012; 3: 401.
136. Delgado T, Carroll PA, Punjabi AS, Margineantu D, Hockenbery DM, Lagunoff M. Induction of the Warburg effect by Kaposi's sarcoma herpesvirus is required for the maintenance of latently infected endothelial cells. Proc Natl Acad Sci USA 2010; 107: 10696-10701.
137. Sanchez EL, Carroll PA, Thalhofer AB, Lagunoff M. Latent KSHV infected endothelial cells are glutamine addicted and require glutaminolysis for survival. PLoS Pathog 2015; 11: e1005052.
138. Delgado T, Sanchez EL, Camarda R, Lagunoff M. Global metabolic profiling of infection by an oncogenic virus: KSHV induces and requires lipogenesis for survival of latent infection. PLoS Pathog 2012; 8: e1002866.
139. Bhatt AP, Jacobs SR, Freemerman AJ, Makowski L, Rathmell JC, Dittmer DP et al. Dysregulation of fatty acid synthesis and glycolysis in non-Hodgkin lymphoma. Proc Natl Acad Sci USA 2012; 109: 11818-11823.
140. Karki R, Lang SM, Means RE. The MARCH family E3 ubiquitin ligase K5 alters monocyte metabolism and proliferation through receptor tyrosine kinase modulation. PLoS Pathog 2011; 7: e1001331.
141. Gandhi MK, Khanna R. Human cytomegalovirus: clinical aspects, immune regulation, and emerging treatments. Lancet Infect Dis 2004; 4: 725-738.
142. Griffiths PD. Burden of disease associated with human cytomegalovirus and prospects for elimination by universal immunisation. Lancet Infect Dis 2012; 12: 790-798.
143. Michaelis M, Doerr HW, Cinatl J. The story of human cytomegalovirus and cancer: increasing evidence and open questions. Neoplasia 2009; 11: 1-9.
144. Harkins L, Volk AL, Samanta M, Mikolaenko I, Britt WJ, Bland KI et al. Specific localisation of human cytomegalovirus nucleic acids and proteins in human colorectal cancer. Lancet 2002; 360: 1557-1563.
145. Prins RM, Cloughesy TF, Liau LM. Cytomegalovirus immunity after vaccination with autologous glioblastoma lysate. N Engl J Med 2008; 359: 539-541.
146. Miller G. Brain cancer. A viral link to glioblastoma? Science 2009; 323: 30-31.
147. Cobbs CS, Harkins L, Samanta M, Gillespie GY, Bharara S, King PH et al. Human cytomegalovirus infection and expression in human malignant glioma. Cancer Res 2002; 62: 3347-3350.
148. Samanta M, Harkins L, Klemm K, Britt WJ, Cobbs CS. High prevalence of human cytomegalovirus in prostatic intraepithelial neoplasia and prostatic carcinoma. J Urol 2003; 170: 998-1002.
149. Price RL, Song J, Bingmer K, Kim TH, Yi JY, Nowicki MO et al. Cytomegalovirus contributes to glioblastoma in the context of tumor suppressor mutations. Cancer Res 2013; 73: 3441-3450.
150. Cinatl J, Scholz M, Kotchetkov R, Vogel JU, Doerr HW. Molecular mechanisms of the modulatory effects of HCMV infection in tumor cell biology. Trends Mol Med 2004; 10: 19-23.
151. Tanaka S, Furukawa T, Plotkin SA. Human cytomegalovirus stimulates host cell RNA synthesis. J Virol 1975; 15: 297-304.
152. Landini MP. Early enhanced glucose uptake in human cytomegalovirusinfected cells. J Gen Virol 1984; 65(Pt 7): 1229-1232.
153. Munger J, Bennett BD, Parikh A, Feng XJ, McArdle J, Rabitz HA et al. Systemslevel metabolic flux profiling identifies fatty acid synthesis as a target for antiviral therapy. Nat Biotechnol 2008; 26: 1179-1186.
154. Munger J, Bajad SU, Coller HA, Shenk T, Rabinowitz JD. Dynamics of the cellular metabolome during human cytomegalovirus infection. PLoS Pathog 2006; 2: e132.
155. Kaarbo M, Ager-Wick E, Osenbroch PO, Kilander A, Skinnes R, Muller F et al. Human cytomegalovirus infection increases mitochondrial biogenesis. Mitochondrion 2011; 11: 935-945.
156. Chambers JW, Maguire TG, Alwine JC. Glutamine metabolism is essential for human cytomegalovirus infection. J Virol 2010; 84: 1867-1873.
157. Spencer CM, Schafer XL, Moorman NJ, Munger J. Human cytomegalovirus induces the activity and expression of acetyl-coenzyme A carboxylase, a fatty acid biosynthetic enzyme whose inhibition attenuates viral replication. J Virol 2011; 85: 5814-5824.
158. Yu Y, Pierciey Jr FJ , Maguire TG, Alwine JC. PKR-like endoplasmic reticulum kinase is necessary for lipogenic activation during HCMV infection. PLoS Pathog 2013; 9: e1003266.
159. Yu Y, Maguire TG, Alwine JC. Human cytomegalovirus infection induces adipocyte-like lipogenesis through activation of sterol regulatory element binding protein 1. J Virol 2012; 86: 2942-2949.
160. McArdle J, Schafer XL, Munger J. Inhibition of calmodulin-dependent kinase kinase blocks human cytomegalovirus-induced glycolytic activation and severely attenuates production of viral progeny. J Virol 2011; 85: 705-714.
161. Clippinger AJ, Maguire TG, Alwine JC. Human cytomegalovirus infection maintains mTOR activity and its perinuclear localization during amino acid deprivation. J Virol 2011; 85: 9369-9376.
162. Yurochko AD. Human Cytomegalovirus Modulation of Signal Transduction. In: Shenk T, Stinski M (eds). Human Cytomegalovirus. Springer: Berlin, Heidelberg, Germany, 2008, pp 205-220.
163. Terry LJ, Vastag L, Rabinowitz JD, Shenk T. Human kinome profiling identifies a requirement for AMP-activated protein kinase during human cytomegalovirus infection. Proc Natl Acad Sci USA 2012; 109: 3071-3076.
164. Yu Y, Maguire TG, Alwine JC. ChREBP, a glucose-responsive transcriptional factor, enhances glucose metabolism to support biosynthesis in human cytomegalovirus-infected cells. Proc Natl Acad Sci USA 2014; 111: 1951-1956.
165. Fontaine KA, Camarda R, Lagunoff M. Vaccinia virus requires glutamine but not glucose for efficient replication. J Virol 2014; 88: 4366-4374.
166. Vastag L, Koyuncu E, Grady SL, Shenk TE, Rabinowitz JD. Divergent effects of human cytomegalovirus and herpes simplex virus-1 on cellular metabolism. PLoS Pathog 2011; 7: e1002124.
167. Birungi G, Chen SM, Loy BP, Ng ML, Li SF. Metabolomics approach for investigation of effects of dengue virus infection using the EA.hy926 cell line. J Proteome Res 2010; 9: 6523-6534.
168. Ritter JB, Wahl AS, Freund S, Genzel Y, Reichl U. Metabolic effects of influenza virus infection in cultured animal cells: Intra- and extracellular metabolite profiling. BMC. Syst Biol 2010; 4: 61.
169. Takahashi M, Wolf AM, Watari E, Norose Y, Ohta S, Takahashi H. Increased mitochondrial functions in human glioblastoma cells persistently infected with measles virus. Antiviral Res 2013; 99: 238-244.
170. Hollenbaugh JA, Munger J, Kim B. Metabolite profiles of human immunodeficiency virus infected CD4+ T cells and macrophages using LC-MS/MS analysis. Virology 2011; 415: 153-159.
171. Sabharwal SS, Schumacker PT. Mitochondrial ROS in cancer: initiators, amplifiers or an Achilles' heel? Nat Rev Cancer 2014; 14: 709-721.
172. Nakamoto Y, Guidotti LG, Kuhlen CV, Fowler P, Chisari FV. Immune pathogenesis of hepatocellular carcinoma. J Exp Med 1998; 188: 341-350.
173. Rickinson AB. Co-infections, inflammation and oncogenesis: future directions for EBV research. Semin Cancer Biol 2014; 26: 99-115.
174. Elinav E, Nowarski R, Thaiss CA, Hu B, Jin C, Flavell RA. Inflammation-induced cancer: crosstalk between tumours, immune cells and microorganisms. Nat Rev Cancer 2013; 13: 759-771.
175. Vander Heiden MG. Targeting cancer metabolism: a therapeutic window opens. Nat Rev Drug Discov 2011; 10: 671-684.
176. DeVita Jr VT, Chu E. A history of cancer chemotherapy. Cancer Res 2008; 68: 8643-8653.
177. De Clercq E. Antivirals and antiviral strategies. Nat Rev Microbiol 2004; 2: 704-720.