Enrichment of stem-like cell population comprises transformation ability of Epstein-Barr virus latent membrane protein 2A for non-transformed cells

Virus Research

Volumn 174, Issue 1-2, 2013, Pages 108-115

  Nakaya, Takeo ^a,b   Kikuchi, Yoshinao ^a   Kunita, Akiko ^a   Ishikawa, Shumpei ^a,c   Matsusaka, Keisuke ^a,c   Hino, Rumi ^a   Aburatani, Hiroyuki ^c   Fukayama, Masashi ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b TOKYO MEDICAL UNIVERSITY   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

Author keywords

Cancer initiating cells; EBV; HMGA2; LMP2A; Oncogenesis; Side population

Indexed keywords

EPSTEIN BARR VIRUS LATENT MEMBRANE PROTEIN 2A; HIGH MOBILITY GROUP A2 PROTEIN; LATENT MEMBRANE PROTEIN 2; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; STAT3 PROTEIN; UNCLASSIFIED DRUG;

AGAR MEDIUM; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER STEM CELL; CELL COUNT; CELL IMMORTALIZATION; CELL LINEAGE; CELL SIZE; CELL STRAIN 3T3; CELL TRANSFORMATION; COLONY FORMATION; CONTROLLED STUDY; ENRICHMENT CULTURE; ENZYME ACTIVATION; EPSTEIN BARR VIRUS; FEMALE; FIBROBLAST; INTRACELLULAR SIGNALING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIDE POPULATION CELL; UPREGULATION; VIRUS CARCINOGENESIS;

ANIMALS; CELL TRANSFORMATION, VIRAL; CELLS, CULTURED; FEMALE; FIBROBLASTS; HERPESVIRUS 4, HUMAN; MICE; MICE, NUDE; STEM CELLS; VIRAL MATRIX PROTEINS;

HUMAN HERPESVIRUS 4; MUS MUSCULUS;

EID: 84877620710     PISSN: 01681702     EISSN: 18727492     Source Type: Journal    
DOI: 10.1016/j.virusres.2013.03.009     Document Type: Article

References (45)

1. Berner J.M., Meza-Zepeda L.A., Kools P.F., Forus A., Schoenmakers E.F., Van de Ven W.J., Fodstad O., Myklebost O. HMGIC, the gene for an architectural transcription factor, is amplified and rearranged in a subset of human sarcomas. Oncogene 1997, 14(24):2935-2941.
2. Caldwell R.G., Wilson J.B., Anderson S.J., Longnecker R. Epstein-Barr virus LMP2A drives B cell development and survival in the absence of normal B cell receptor signals. Immunity 1998, 9(3):405-411.
3. Chen S.Y., Lu J., Shih Y.C., Tsai C.H. Epstein-Barr virus latent membrane protein 2A regulates c-jun protein through extracellular signal-regulated kinase. Journal of Virology 2002, 76(18):9556-9561.
4. Dean M., Fojo T., Bates S. Tumour stem cells and drug resistance. Nature Reviews Cancer 2005, 5(4):275-284.
5. Eisenhoffer G.T., Loftus P.D., Yoshigi M., Otsuna H., Chien C.B., Morcos P.A., Rosenblatt J. Crowding induces live cell extrusion to maintain homeostatic cell numbers in epithelia. Nature 2012, 484(7395):546-549.
6. Fukayama M., Chong J.M., Uozaki H. Pathology and molecular pathology of Epstein-Barr virus-associated gastric carcinoma. Current Opinion in Microbiology and Immunology 2001, 258:91-102.
7. Fukayama M., Hayashi Y., Iwasaki Y., Chong J., Ooba T., Takizawa T., Koike M., Mizutani S., Miyaki M., Hirai K. Epstein-Barr virus-associated gastric carcinoma and Epstein-Barr virus infection of the stomach. Laboratory Investigation 1994, 71(1):73-81.
8. Fukayama M., Hino R., Uozaki H. Epstein-Barr virus and gastric carcinoma: virus-host interactions leading to carcinoma. Cancer Science 2008, 99(9):1726-1733.
9. Fukayama M., Ushiku T. Epstein-Barr virus-associated gastric carcinoma. Pathology, Research and Practice 2011, 207(9):529-537.
10. Fukuda M., Longnecker R. Epstein-Barr virus latent membrane protein 2A mediates transformation through constitutive activation of the Ras/PI3-K/Akt Pathway. Journal of Virology 2007, 81(17):9299-9306.
11. Hadnagy A., Gaboury L., Beaulieu R., Balicki D. SP analysis might be used to identify cancer stem cell populations. Experimental Cell Research 2006, 312(19):3701-3710.
12. Hino R., Uozaki H., Murakami N., Ushiku T., Shinozaki A., Ishikawa S., Morikawa T., Nakaya T., Sakatani T., Takada K., Fukayama M. Activation of DNA methyltransferase 1 by EBV latent membrane protein 2A leads to promoter hypermethylation of PTEN gene in gastric carcinoma. Cancer Research 2009, 69(7):2766-2774.
13. Hirschmann-Jax C., Foster A.E., Wulf G.G., Nuchtern J.G., Jax T.W., Gobel U., Goodell M.A., Brenner M.K. A distinct "side population" of cells with high drug efflux capacity in human tumor cells. Proceedings of National Academy of Science of United states of America 2004, 101(39):14228-14233.
14. Kitamura T. New experimental approaches in retrovirus-mediated expression screening. International Journal of Hematology 1998, 67(4):351-359.
15. Kondo S., Wakisaka N., Muramatsu M., Zen Y., Endo K., Murono S., Sugimoto H., Yamaoka S., Pagano J.S., Yoshizaki T. Epstein-Barr virus latent membrane protein 1 induces cancer stem/progenitor-like cells in nasopharyngeal epithelial cell lines. Journal of Virology 2011, 85(21):11255-11264.
16. Kong Q.L., Hu L.J., Cao J.Y., Huang Y.J., Xu L.H., Liang Y., Xiong D., Guan S., Guo B.H., Mai H.Q., Chen Q.Y., Zhang X., Li M.Z., Shao J.Y., Qian C.N., Xia Y.F., Song L.B., Zeng Y.X., Zeng M.S. Epstein-Barr virus-encoded LMP2A induces an epithelial-mesenchymal transition and increases the number of side population stem-like cancer cells in nasopharyngeal carcinoma. PLoS Pathogens 2010, 6(6):e1000940.
17. Lan Y.Y., Hsiao J.R., Chang K.C., Chang J.S., Chen C.W., Lai H.C., Wu S.Y., Yeh T.H., Chang F.H., Lin W.H., Su I.J., Chang Y. Epstein-Barr virus latent membrane protein 2A promotes invasion of nasopharyngeal carcinoma cells through ERK/Fra-1-mediated induction of matrix metalloproteinase 9. Journal of Virology 2012, 86(12):6656-6667.
18. Lee Y.S., Dutta A. The tumor suppressor microRNA let-7 represses the HMGA2 oncogene. Genes and Development 2007, 21(9):1025-1030.
19. Longnecker R. Biochemical and genetic studies of Epstein-Barr virus latent membrane protein 2. Leukemia 1994, 8(Suppl. 11):S46-S50.
20. Lopez-Garcia C., Klein A.M., Simons B.D., Winton D.J. Intestinal stem cell replacement follows a pattern of neutral drift. Science 2010, 330(6005):822-825.
21. Marinari E., Mehonic A., Curran S., Gale J., Duke T., Baum B. Live-cell delamination counterbalances epithelial growth to limit tissue overcrowding. Nature 2012, 484(7395):542-545.
22. Matsusaka K., Kaneda A., Nagae G., Ushiku T., Kikuchi Y., Hino R., Uozaki H., Seto Y., Takada K., Aburatani H., Fukayama M. Classification of Epstein-Barr virus-positive gastric cancers by definition of DNA methylation epigenotypes. Cancer Research 2011, 71(23):7187-7197.
23. Mayr C., Hemann M.T., Bartel D.P. Disrupting the pairing between let-7 and Hmga2 enhances oncogenic transformation. Science 2007, 315(5818):1576-1579.
24. McCoy M.S., Toole J.J., Cunningham J.M., Chang E.H., Lowy D.R., Weinberg R.A. Characterization of a human colon/lung carcinoma oncogene. Nature 1983, 302(5903):79-81.
25. Morrison J.A., Raab-Traub N. Roles of the ITAM and PY motifs of Epstein-Barr virus latent membrane protein 2A in the inhibition of epithelial cell differentiation and activation of {beta}-catenin signaling. Journal of Virology 2005, 79(4):2375-2382.
26. Motoyama K., Inoue H., Nakamura Y., Uetake H., Sugihara K., Mori M. Clinical significance of high mobility group A2 in human gastric cancer and its relationship to let-7 microRNA family. Clinical Cancer Research 2008, 14(8):2334-2340.
27. Nakatani Y., Ogryzko V. Immunoaffinity purification of mammalian protein complexes. Methods in Enzymology 2003, 370:430-444.
28. Nishino J., Kim I., Chada K., Morrison S.J. Hmga2 promotes neural stem cell self-renewal in young but not old mice by reducing p16Ink4a and p19Arf Expression. Cell 2008, 135(2):227-239.
29. Patrawala L., Calhoun T., Schneider-Broussard R., Zhou J., Claypool K., Tang D.G. Side population is enriched in tumorigenic, stem-like cancer cells, whereas ABCG2+ and ABCG2- cancer cells are similarly tumorigenic. Cancer Research 2005, 65(14):6207-6219.
30. Reeves R. Molecular biology of HMGA proteins: hubs of nuclear function. Gene 2001, 277(1-2):63-81.
31. Scholle F., Bendt K.M., Raab-Traub N. Epstein-Barr virus LMP2A transforms epithelial cells, inhibits cell differentiation, and activates Akt. Journal of Virology 2000, 74(22):10681-10689.
32. Siler C.A., Raab-Traub N. Rhesus lymphocryptovirus latent membrane protein 2A activates beta-catenin signaling and inhibits differentiation in epithelial cells. Virology 2008, 377(2):273-279.
33. Snippert H.J., van der Flier L.G., Sato T., van Es J.H., van den Born M., Kroon-Veenboer C., Barker N., Klein A.M., van Rheenen J., Simons B.D., Clevers H. Intestinal crypt homeostasis results from neutral competition between symmetrically dividing Lgr5 stem cells. Cell 2010, 143(1):134-144.
34. Stewart S., Dawson C.W., Takada K., Curnow J., Moody C.A., Sixbey J.W., Young L.S. Epstein-Barr virus-encoded LMP2A regulates viral and cellular gene expression by modulation of the NF-kappaB transcription factor pathway. Proceedings of National Academy of Science of United states of America 2004, 101(44):15730-15735.
35. Takada K. Epstein-Barr virus and gastric carcinoma. Molecular Pathology 2000, 53(5):255-261.
36. Thuault S., Tan E.J., Peinado H., Cano A., Heldin C.H., Moustakas A. HMGA2 and Smads co-regulate SNAIL1 expression during induction of epithelial-to-mesenchymal transition. Journal of Biological Chemistry 2008, 283(48):33437-33446.
37. Thuault S., Valcourt U., Petersen M., Manfioletti G., Heldin C.H., Moustakas A. Transforming growth factor-beta employs HMGA2 to elicit epithelial-mesenchymal transition. Journal of Cell Biology 2006, 174(2):175-183.
38. Tsuei D.J., Hsu H.C., Lee P.H., Jeng Y.M., Pu Y.S., Chen C.N., Lee Y.C., Chou W.C., Chang C.J., Ni Y.H., Chang M.H. RBMY, a male germ cell-specific RNA-binding protein, activated in human liver cancers and transforms rodent fibroblasts. Oncogene 2004, 23(34):5815-5822.
39. Turkson J., Zhang S., Mora L.B., Burns A., Sebti S., Jove R. A novel platinum compound inhibits constitutive Stat3 signaling and induces cell cycle arrest and apoptosis of malignant cells. Journal of Biological Chemistry 2005, 280(38):32979-32988.
40. Wang J., Guo L.P., Chen L.Z., Zeng Y.X., Lu S.H. Identification of cancer stem cell-like side population cells in human nasopharyngeal carcinoma cell line. Cancer Research 2007, 67(8):3716-3724.
41. Watanabe S., Ueda Y., Akaboshi S., Hino Y., Sekita Y., Nakao M. HMGA2 maintains oncogenic RAS-induced epithelial-mesenchymal transition in human pancreatic cancer cells. American Journal of Pathology 2009, 174(3):854-868.
42. Young A.R., Narita M. Oncogenic HMGA2: short or small?. Genes and Development 2007, 21(9):1005-1009.
43. Young L.S., Rickinson A.B. Epstein-Barr virus: 40 years on. Nature Reviews Cancer 2004, 4(10):757-768.
44. Zhou J., Wulfkuhle J., Zhang H., Gu P., Yang Y., Deng J., Margolick J.B., Liotta L.A., Petricoin E., Third, Zhang Y. Activation of the PTEN/mTOR/STAT3 pathway in breast cancer stem-like cells is required for viability and maintenance. Proceedings of National Academy of Science of United states of America 2007, 104(41):16158-16163.
45. Zhou S., Schuetz J.D., Bunting K.D., Colapietro A.M., Sampath J., Morris J.J., Lagutina I., Grosveld G.C., Osawa M., Nakauchi H., Sorrentino B.P. The ABC transporter Bcrp1/ABCG2 is expressed in a wide variety of stem cells and is a molecular determinant of the side-population phenotype. Nature Medicine 2001, 7(9):1028-1034.