EB-virus latent membrane protein 1 potentiates the stemness of nasopharyngeal carcinoma via preferential activation of PI3K/AKT pathway by a positive feedback loop

Oncogene

Volumn 35, Issue 26, 2016, Pages 3419-3431

  Yang, C F ^a,b   Yang, G D ^c   Huang, T J ^d   Li, R ^e   Chu, Q Q ^c   Xu, L ^a   Wang, M S ^b   Cai, M D ^b   Zhong, L ^b   Wei, H J ^b   Huang, H B ^a   Huang, J L ^f   Qian, C N ^a   Huang, B J ^a  

^a SUN YAT SEN UNIVERSITY CANCER CENTER   (China)

^b GUANGDONG PROVINCIAL PEOPLE'S HOSPITAL   (China)

^c SUN YAT SEN UNIVERSITY   (China)

^d SECOND PEOPLE S HOSPITAL OF SHENZHEN   (China)

^e SOUTHERN MEDICAL UNIVERSITY   (China)

^f SAINT BARNABAS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BMI1 PROTEIN; BREAST CANCER RESISTANCE PROTEIN; CYTOKERATIN 14; CYTOKERATIN 18; CYTOKERATIN 19; GELATINASE B; HERMES ANTIGEN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; LATENT MEMBRANE PROTEIN 1; MICRORNA 21; OCTAMER TRANSCRIPTION FACTOR 4; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PHOSPHORYLASE; PROTEIN KINASE B; STROMELYSIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR ZEB2; UNCLASSIFIED DRUG; UVOMORULIN; VASCULOTROPIN; VIMENTIN; EBV-ASSOCIATED MEMBRANE ANTIGEN, EPSTEIN-BARR VIRUS; MATRIX PROTEIN; MICRORNA; MIRN21 MICRORNA, HUMAN; PTEN PROTEIN, HUMAN;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CANCER STEM CELL; CELL DIFFERENTIATION; CONTROLLED STUDY; DOWN REGULATION; ENZYME PHOSPHORYLATION; EPITHELIAL MESENCHYMAL TRANSITION; EPSTEIN BARR VIRUS; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; MOUSE; NASOPHARYNX CARCINOMA; NONHUMAN; POSITIVE FEEDBACK; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; UPREGULATION; ADULT; AGED; ANIMAL; BAGG ALBINO MOUSE; CELL LINE; FEMALE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOBLOTTING; MALE; METABOLISM; MIDDLE AGED; NASOPHARYNX TUMOR; NUDE MOUSE; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TUMOR CELL LINE; XENOGRAFT;

ADULT; AGED; ANIMALS; CELL LINE; CELL LINE, TUMOR; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOBLOTTING; MALE; MICE, INBRED BALB C; MICE, NUDE; MICRORNAS; MIDDLE AGED; NASOPHARYNGEAL NEOPLASMS; NEOPLASTIC STEM CELLS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; PTEN PHOSPHOHYDROLASE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSPLANTATION, HETEROLOGOUS; VIRAL MATRIX PROTEINS;

EID: 84976906513     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2015.402     Document Type: Article

References (51)

1. Chew MM, Gan SY, Khoo AS, Tan EL. Interleukins, laminin and Epstein-Barr virus latent membrane protein 1 (EBV LMP1) promote metastatic phenotype in nasopharyngeal carcinoma. BMC Cancer 2010; 10: 574.
2. Young LS, Rickinson AB. Epstein-Barr virus: 40 years. Nat Rev Cancer 2004; 4: 757-768.
3. 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.
4. Yang CF, Peng LX, Yang GD, Yang GD, Chu QQ, Liang YY et al. Cancer stem-like cell characteristics induced by EB virus-encoded LMP1 contribute to radioresistance in nasopharyngeal carcinoma by suppressing the p53-mediated apoptosis pathway. Cancer Lett 2014; 344: 260-271.
5. Frank NY, Schatton T, Frank MH. The therapeutic promise of the cancer stem cell concept. J Clin Invest 2010; 120: 41-50.
6. Prince ME, Ailles LE. Cancer stem cells in head and neck squamous cell cancer. J Clin Oncol 2008; 26: 2871-2875.
7. Chen JZ. Roles of the PI3K/Akt pathway in Epstein-Barr virus-induced cancers and therapeutic implications. World J Virol 2012; 12: 154-161.
8. Mainou BA, Everly DN, Raab TN. Epstein-Barr virus latent membrane protein 1 CTAR1 mediates rodent and human fibroblast transformation through activation of PI3K. Oncogene 2005; 24: 6917-6924.
9. Dubrovska A, Kim S, Salamone RJ, Walker JR, Maira SM, García-Echeverría C et al. The role of PTEN/Akt/PI3K signaling in the maintenance and viability of prostate cancer stem-like cell populations. Proc Natl Acad Sci USA 2009; 106: 268-273.
10. Lambert SL, Martinez OM. Latent membrane protein 1 of EBV activates phosphatidylinositol 3-kinase to induce production of IL-10. J Immunol 2007; 179: 8225-8234.
11. 3a pathway in human epithelial cells. J Virol 2008; 82: 8124-8137.
12. Yang GD, Huang TJ, Peng LX, Yang CF, Liu RY, Huang HB et al. Epstein-Barr Virus-Encoded LMP1 upregulates microRNA-21 to promote the resistance of nasopharyngeal carcinoma cells to cisplatin-induced apoptosis by suppressing PDCD4 and Fas-L. PLoS One 2013; 8: e78355.
13. Lee JW, Liu PF, Hsu LP, Chen PR, Chang CH, Shih WL. EBV LMP-1 negatively regulates expression and pro-apoptotic activity of Par-4 in nasopharyngeal carcinoma cells. Cancer Lett 2009; 279: 193-201.
14. Cancer Genome Atlas Research Network. Comprehensive molecular characterization of clear cell renal cell carcinoma. Nature 2013; 499: 43-49.
15. Sendurai AM, Wen JG, Mai JL, Eaton EN, Ayyanan A, Zhou AY et al. The epithelialmesenchymal transition generates cells with properties of stem cells. Cell 2008; 133: 704-715.
16. Antonio DC, Pier PP. The multiple roles of PTEN in tumor suppression. Cell 2000; 100: 387-390.
17. Groszer M, Erickson R, Scripture-Adams DD, Lesche R, Trumpp A, Zack JA et al. Negative regulation of neural stem/progenitor cell proliferation by the Pten tumor suppressor gene in vivo. Science 2001; 294: 2186-2189.
18. Bonnet D, Dick JE. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 1997; 3: 730-737.
19. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J et al. Identification of a cancer stem cell in human brain tumors. Cancer Res 2003; 63: 5821-5828.
20. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 2003; 100: 3983-3988.
21. Takaishi S, Okumura T, Tu S, Wang SS, Shibata W, Vigneshwaran R et al. Identification of gastric cancer stem cells using the cell surface marker CD44. Stem Cells 2009; 27: 1006-1020.
22. Prince ME, Sivanandan R, Kaczorowski A, Wolf GT, Kaplan MJ, Dalerba P et al. Identifcation of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma. Proc Natl Acad Sci USA 2007; 104: 973-978.
23. Patrawala L, Calhoun T, Schneider-Broussard R, Li H, Bhatia B, Tang S et al. Highly purified CD44+ prostate cancer cells from xenograft human tumors are enriched in tumorigenic and metastatic progenitor cells. Oncogene 2006; 25: 1696-1708.
24. Li C, Heidt DG, Dalerba P, Burant CF, Zhang L, Adsay V et al. Identification of pancreatic cancer stem cells. Cancer Res 2007; 67: 1030-1037.
25. Dalerba P, Dylla SJ, Park IK, Liu R, Wang X, Cho RW, et al. Phenotypic characterization of human colorectal cancer stem cells. Proc Natl Acad Sci USA 2007b; 104: 10158-10163.
26. Kondo S, Wakisaka N, Muramatsu M, Zen Y, Endo K, Murono S et al. Epstein-Barr virus latent membrane protein 1 induces cancer stem/progenitor-like cells in nasopharyngeal epithelial cell lines. J Virol 2011; 85: 11255-11264.
27. Tellez CS, Juri DE, Do K, Bernauer AM, Thomas CL, Damiani LA et al. EMT and stem cell-like properties associated with miR-205 and miR-200 epigenetic silencing are early manifestations during carcinogen-induced transformation of human lung epithelial cells. Cancer Res 2011; 71: 3087-3097.
28. Swapna A, Kiran KV, Chandramu C, Bharathi Go, Jasti SR. Epigenetic regulation of miRNA-211 by MMP-9 governs glioma cell apoptosis, chemosensitivity and radiosensitivity. Oncotarget 2012; 3: 1439-1454.
29. Bao B, Azmi AS, Ali S, Ahmad A, Li Y, Banerjee S et al. The biological kinship of hypoxia with CSC and EMT and their relationship with deregulated expression of miRNAs and tumor aggressiveness. Biochim Biophys Acta 2012; 1826: 272-296.
30. Adele H, Joanna BW. Evaluation of LMP1 of Epstein-Barr virus as a therapeutic target by its inhibition. Mol Cancer 2010; 9: 184.
31. Ma S, Lee TK, Zheng BJ, Chan KW, Guan XY. CD133+ HCC cancer stem cells confer chemoresistance by preferential expression of the Akt/PKB survival pathway. Oncogene 2008; 27: 1749-1758.
32. Qian CN, Furge KA, Knol J, Huang D, Chen J, Dykema KJ et al. Activation of the PI3K/ AKT pathway induces urothelial carcinoma of the renal pelvis: identification in human tumors and confirmation in animal models. Cancer Res 2009; 69: 8256-8264.
33. Dubrovska A, Elliott J, Salamone RJ, Kim S, Aimone LJ, Walker JR et al. Combination therapy targeting both tumor-initiating and differentiated cell populations in prostate carcinoma. Clin Cancer Res 2010; 16: 5692-5702.
34. Lavorgna A, Harhaj EW. EBV LMP1: new and shared pathways to NF-κB activation. Proc Natl Acad Sci USA 2012; 109: 2188-2189.
35. Xishan Z, Xinna Z, Baoxin H, Jun R. Impaired immunomodulatory function of chronic myeloid leukemia cancer stem cells and the possible mechanism involved in it. Cancer Immunol Immunother 2013; 62: 689-703.
36. Chen CC, Chen LC, Liang Y, Tsang NM, Chang YS. Epstein-Barr virus latent membrane protein 1 induces the chemotherapeutic target, thymidine phosphorylase, via NF-kappaB and p38 MAPK pathways. Cell Signal 2010; 22: 1132-1142.
37. Kutz H, Reisbach G, Schultheiss U, Kieser A. The c-Jun N-terminal kinase pathway is critical for cell transformation by the latent membrane protein 1 of Epstein-Barr virus. Virology 2008; 371: 246-256.
38. Volinia S, Calin GA, Liu CG, Ambs S, Cimmino A, Petrocca F et al. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci USA 2006; 103: 2257-2261.
39. Gong C, Yao Y, Wang Y, Liu B, Wu W, Chen J et al. Upregulation of MIR-21 mediates resistance to trastuzumab therapy for breast cancer. J Biol Chem 2011; 286: 19127-19137.
40. Meng F, Henson R, Wehbe JH, Ghoshal K, Jacob ST, Patel T. MicroRNA-21 regulates expression of the PTEN tumor suppressor gene in human hepatocellular cancer. Gastroenterology 2007; 133: 647-658.
41. Asangani IA, Rasheed SA, Nikolova DA, Leupold JH, Colburn NH, Post S et al. MicroRNA-21 (miR-21) post-transcriptionally downregulates tumor suppressor Pdcd4 and stimulates invasion, intravasation and metastasis in colorectal cancer. Oncogene 2008; 27: 2128-2136.
42. Yamamoto C, Basaki Y, Kawahara A, Nakashima K, Kage M, Izumi H et al. Loss of PTEN expression by blocking nuclear translocation of EGR1 in gefitinib-resistant lung cancer cells harboring epidermal growth factor receptor-activating mutations. Cancer Res 2010; 70: 8715-8725.
43. Longlong Bao. MicroRNA-21 suppresses PTEN and hSulf-1 expression and promotes hepatocellular carcinoma progression through AKT/ERK pathways. Cancer Lett 2013; 337: 226-236.
44. Zhu S, Wu H, Wu F, Nie D, Sheng S, Mo YY. MicroRNA-21 targets tumor suppressor genes in invasion and metastasis. Cell Res 2008; 18: 350-359.
45. Castellino RC, Durden DL. Mechanisms of Disease: the PI3K-Akt-PTEN signaling node an intercept point for the control of angiogenesis in brain tumors. Nat Clin Pract Neurol 2007; 3: 682-693.
46. Sayed D, He M, Hong C, Gao S, Rane S, Yang Z et al. MicroRNA-21 is a downstream effector of AKT that mediates its antiapoptotic effects via suppression of Fas ligand. J Biol Chem 2010; 285: 20281-20290.
47. Yang SM, Huang C, Li XF, Yu MZ, He Y, Li J. miR-21 confers cisplatin resistance in gastric cancer cells by regulating PTEN. Toxicology 2013; 306: 162-168.
48. Pedrero JM, Carracedo DG, Pinto CM, Zapatero AH, Rodrigo JP, Nieto CS et al. Frequent genetic and biochemical alterations of the PI 3-K/AKT/PTEN pathway in head and neck squamous cell carcinoma. Int J Cancer 2005; 114: 242-248.
49. Han M, Wang Y, Liu M, Bi X, Bao J, Zeng N et al. MiR-21 regulates epithelialmesenchymal transition phenotype and hypoxia-inducible factor-1alpha expression in third-sphere forming breast cancer stem cell-like cells. Cancer Sci 2012; 4: 1058-1064.
50. Selcuklu SD, Donoghue MT, Spillane C. miR-21 as a key regulator of oncogenic processes. Biochem Soc Trans 2009; 4: 918-925.
51. Chung WM, Chang WC, Chen L, Chang YY, Shyr CR, Hung YC et al. MicroRNA-21 promotes the ovarian teratocarcinoma PA1 cell line by sustaining cancer stem/ progenitor populations in vitro. Stem Cell Res Ther 2013; 4: 88.