Targeting Epstein-Barr virus oncoprotein LMP1-mediated glycolysis sensitizes nasopharyngeal carcinoma to radiation therapy

Oncogene

Volumn 33, Issue 37, 2014, Pages 4568-4578

  Xiao, L ^a,b,c   Hu, Z Y ^a,b,c,d   Dong, X ^a,b,c   Tan, Z ^a,b,c   Li, W ^a,b,c   Tang, M ^a,b,c,d   Chen, L ^a,b,c   Yang, L ^a,b,c,f   Tao, Y ^a,b,c   Jiang, Y ^a,b,c   Li, J ^a,b,c   Yi, B ^f   Li, B ^f   Fan, S ^e   You, S ^e,g   Deng, X ^g   Hu, F ^e   Feng, L ^e   Bode, A M ^h   Dong, Z ^h   Sun, L Q ^f   Cao, Y ^a,b,c   more..

^a Central South University   (China)

^b BEIJING UNIVERSITY OF POSTS AND TELECOMMUNICATIONS   (China)

^c BEIJING HOSPITAL   (China)

^d First Hospital of Changsha City   (China)

^e CENTRAL SOUTH UNIVERSITY   (China)

^f CENTRAL SOUTH UNIVERSITY   (China)

^g EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^h UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EBV ASSOCIATED MEMBRANE ANTIGEN, EPSTEIN BARR VIRUS; EBV-ASSOCIATED MEMBRANE ANTIGEN, EPSTEIN-BARR VIRUS; GLUCOSE; HEXOKINASE; LACTIC ACID; MATRIX PROTEIN; MYC PROTEIN; RADIOSENSITIZING AGENT;

APOPTOSIS; ARTICLE; CELL PROLIFERATION; CELL SURVIVAL; CHEMISTRY; EPSTEIN BARR VIRUS; GENE EXPRESSION REGULATION; GLYCOLYSIS; HUMAN; METABOLISM; METABOLOMICS; NASOPHARYNX CARCINOMA; NASOPHARYNX TUMOR; SIGNAL TRANSDUCTION; TUMOR CELL LINE; VIROLOGY;

APOPTOSIS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE EXPRESSION REGULATION, VIRAL; GLUCOSE; GLYCOLYSIS; HERPESVIRUS 4, HUMAN; HEXOKINASE; HUMANS; LACTIC ACID; METABOLOMICS; NASOPHARYNGEAL NEOPLASMS; PROTO-ONCOGENE PROTEINS C-MYC; RADIATION-SENSITIZING AGENTS; SIGNAL TRANSDUCTION; VIRAL MATRIX PROTEINS;

EID: 84896421900     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2014.32     Document Type: Article

References (45)

1. Koppenol WH, Bounds PL, Dang CV. Otto Warburg's contributions to current concepts of cancer metabolism. Nat Rev Cancer 2011; 11: 325-337.
2. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011; 144: 646-674.
3. Noch E, Khalili K. Oncogenic viruses and tumor glucose metabolism: like kids in a candy store. Mol Cancer Ther 2012; 11: 14-23.
4. Young LS, Rickinson AB. Epstein-Barr virus: 40 years on. Nat Rev Cancer 2004; 4: 757-768.
5. Ascherio A, Munger KL. Epstein-barr virus infection and multiple sclerosis: a review. J Neuroimmune Pharmacol 2010; 5: 271-277.
6. 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.
7. Zheng H, Li LL, Hu DS, Deng XY, Cao Y. Role of Epstein-Barr virus encoded latent membrane protein 1 in the carcinogenesis of nasopharyngeal carcinoma. Cell Mol Immunol 2007; 4: 185-196.
8. Ma X, Yang L, Xiao L, Tang M, Liu L, Li Z et al. Down-regulation of EBV-LMP1 radiosensitizes nasal pharyngeal carcinoma cells via NF-kappaB regulated ATM expression. PloS One 2011; 6: e24647.
9. Lu ZX, Ma XQ, Yang LF, Wang ZL, Zeng L, Li ZJ et al. DNAzymes targeted to EBV-encoded latent membrane protein-1 induce apoptosis and enhance radiosensitivity in nasopharyngeal carcinoma. Cancer Lett 2008; 265: 226-238.
10. Yecies JL, Manning BD. Transcriptional control of cellular metabolism by mTOR signaling. Cancer Res 2011; 71: 2815-2820.
11. Wallace DC. Mitochondria and cancer: Warburg addressed. Cold Spring Harb Symp Quant Biol 2005; 70: 363-374.
12. Pastorino JG, Shulga N, Hoek JB. Mitochondrial binding of hexokinase II inhibits Bax-induced cytochrome c release and apoptosis. J Biol Chem 2002; 277: 7610-7618.
13. Majewski N, Nogueira V, Bhaskar P, Coy PE, Skeen JE, Gottlob K et al. Hexokinasemitochondria interaction mediated by Akt is required to inhibit apoptosis in the presence or absence of Bax and Bak. Mol Cell 2004; 16: 819-830.
14. Terrin L, Dal Col J, Rampazzo E, Zancai P, Pedrotti M, Ammirabile G et al. Latent membrane protein 1 of Epstein-Barr virus activates the hTERT promoter and enhances telomerase activity in B lymphocytes. J Virol 2008; 82: 10175-10187.
15. Welcker M, Clurman BE. FBW7 ubiquitin ligase: a tumour suppressor at the crossroads of cell division, growth and differentiation. Nat Rev Cancer 2008; 8: 83-93.
16. Soni V, Cahir-McFarland E, Kieff E. LMP1 TRAFficking activates growth and survival pathways. Adv Exp Med Biol 2007; 597: 173-187.
17. 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.
18. Sommermann TG, O'Neill K, Plas DR, Cahir-McFarland E. IKKbeta and NF-kappaB transcription govern lymphoma cell survival through AKT-induced plasma membrane trafficking of GLUT1. Cancer Res 2011; 71: 7291-7300.
19. Shin HJ, Park YH, Kim SU, Moon HB, Park do S, Han YH et al. Hepatitis B virus X protein regulates hepatic glucose homeostasis via activation of inducible nitric oxide synthase. J Biol Chem 2011; 286: 29872-29881.
20. 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.
21. 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.
22. 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.
23. 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.
24. Kohio HP, Adamson AL. Glycolytic control of vacuolar-type ATPase activity: a mechanism to regulate influenza viral infection. Virology 2013; 444: 301-309.
25. Xu W, Yang H, Liu Y, Yang Y, Wang P, Kim SH et al. Oncometabolite 2-hydroxyglutarate is a competitive inhibitor of alpha-ketoglutarate-dependent dioxygenases. Cancer Cell 2011; 19: 17-30.
26. Yang W, Xia Y, Hawke D, Li X, Liang J, Xing D et al. PKM2 phosphorylates histone H3 and promotes gene transcription and tumorigenesis. Cell 2012; 150: 685-696.
27. Patra KC, Wang Q, Bhaskar PT, Miller L, Wang Z, Wheaton W et al. Hexokinase 2 is required for tumor initiation and maintenance and its systemic deletion is therapeutic in mouse models of cancer. Cancer Cell 2013; 24: 213-228.
28. Liu WS, Wu MF, Tseng HC, Liu JT, Weng JH, Li YC et al. The role of pretreatment FDG-PET in nasopharyngeal carcinoma treated with intensity-modulated radiotherapy. Int J Radiat Oncol Biol Phys 2012; 82: 561-566.
29. Tang LQ, Chen QY, Fan W, Liu H, Zhang L, Guo L et al. Prospective study of tailoring whole-body dual-modality [18F]fluorodeoxyglucose positron emission tomography/computed tomography with plasma Epstein-Barr virus DNA for detecting distant metastasis in endemic nasopharyngeal carcinoma at initial staging. J Clin Oncol 2013; 31: 2861-2869.
30. Chen JQ, Russo J. Dysregulation of glucose transport, glycolysis, TCA cycle and glutaminolysis by oncogenes and tumor suppressors in cancer cells. Biochim Biophys Acta 2012; 1826: 370-384.
31. 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.
32. Levine AJ, Puzio-Kuter AM. The control of the metabolic switch in cancers by oncogenes and tumor suppressor genes. Science 2010; 330: 1340-1344.
33. Agrawal N, Frederick MJ, Pickering CR, Bettegowda C, Chang K, Li RJ et al. Exome sequencing of head and neck squamous cell carcinoma reveals inactivating mutations in NOTCH1. Science 2011; 333: 1154-1157.
34. Shair KH, Bendt KM, Edwards RH, Bedford EC, Nielsen JN, Raab-Traub N. EBV latent membrane protein 1 activates Akt, NFkappaB, and Stat3 in B cell lymphomas. PLoS Pathog 2007; 3: e166.
35. Mainou BA, Everly Jr DN, Raab-Traub N. Epstein-Barr virus latent membrane protein 1 CTAR1 mediates rodent and human fibroblast transformation through activation of PI3K. Oncogene 2005; 24: 6917-6924.
36. Meckes Jr DG, Menaker NF, Raab-Traub N. EBV LMP1 modulates lipid raft microdomains and the vimentin cytoskeleton for signal transduction and transformation. J Virol 2012; 87: 1301-1311.
37. Kim JW, Gao P, Liu YC, Semenza GL, Dang CV. Hypoxia-inducible factor 1 and dysregulated c-Myc cooperatively induce vascular endothelial growth factor and metabolic switches hexokinase 2 and pyruvate dehydrogenase kinase 1. Mol Cell Biol 2007; 27: 7381-7393.
38. Wakisaka N, Kondo S, Yoshizaki T, Murono S, Furukawa M, Pagano JS. Epstein-Barr virus latent membrane protein 1 induces synthesis of hypoxia-inducible factor 1 alpha. Mol Cell Biol 2004; 24: 5223-5234.
39. Kondo S, Seo SY, Yoshizaki T, Wakisaka N, Furukawa M, Joab I et al. EBV latent membrane protein 1 up-regulates hypoxia-inducible factor 1alpha through Siah1- mediated down-regulation of prolyl hydroxylases 1 and 3 in nasopharyngeal epithelial cells. Cancer Res 2006; 66: 9870-9877.
40. Yuan S, Fu Y, Wang X, Shi H, Huang Y, Song X et al. Voltage-dependent anion channel 1 is involved in endostatin-induced endothelial cell apoptosis. FASEB J 2008; 22: 2809-2820.
41. Gimenez-Cassina A, Lim F, Cerrato T, Palomo GM, Diaz-Nido J. Mitochondrial hexokinase II promotes neuronal survival and acts downstream of glycogen synthase kinase-3. J Biol Chem 2009; 284: 3001-3011.
42. Reitman ZJ, Jin G, Karoly ED, Spasojevic I, Yang J, Kinzler KW et al. Profiling the effects of isocitrate dehydrogenase 1 and 2 mutations on the cellular metabolome. Proc Natl Acad Sci USA 2011; 108: 3270-3275.
43. Yang H, Bocchetta M, Kroczynska B, Elmishad AG, Chen Y, Liu Z et al. TNF-alpha inhibits asbestos-induced cytotoxicity via a NF-kappaB-dependent pathway, a possible mechanism for asbestos-induced oncogenesis. Proc Natl Acad Sci USA 2006; 103: 10397-10402.
44. Marquitz AR, Mathur A, Shair KH, Raab-Traub N. Infection of Epstein-Barr virus in a gastric carcinoma cell line induces anchorage independence and global changes in gene expression. Proc Natl Acad Sci USA 2012; 109: 9593-9598.
45. Hu J, Deng X, Bian X, Li G, Tong Y, Li Y et al. The expression of functional chemokine receptor CXCR4 is associated with the metastatic potential of human nasopharyngeal carcinoma. Clin Cancer Res 2005; 11: 4658-4665.