1887

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Volume 94, Issue 3

Upregulation of special AT-rich-binding protein 1 by Epstein–Barr virus latent membrane protein 1 in human nasopharyngeal cells and nasopharyngeal cancer Free

Abstract

A global regulator of chromatin remodelling and gene expression, special AT-rich-binding protein 1 (SATB1) has been implicated in promotion of growth and metastasis of a number of cancers. Here, we demonstrate that the principal oncogene of Epstein–Barr virus (EBV), latent membrane protein 1 (LMP1) upregulates SATB1 RNA and protein expression in human nasopharyngeal cell lines. Silencing of endogenously expressed SATB1 with specific short hairpin RNA decreases cell proliferation and resistance to apoptosis induced by growth factor withdrawal. Additionally, we provide evidence that LMP1-mediated expression of Survivin, a multifunctional protein involved in promoting cell growth and survival, is mediated at least in part by SATB1 in human nasopharyngeal cells. Finally, we show that SATB1 protein levels are elevated in tissue samples from patients with nasopharyngeal carcinoma (NPC), and are directly correlated with the expression of LMP1. Taken together, our results suggest that SATB1 functions as a pro-metastatic effector of LMP1 signalling in EBV-positive NPC.

  • Received:
  • Accepted:
  • Published Online:
© 2013 SGM
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2013-03-01
2024-04-27
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References

  1. Agrelo R., Wutz A. 2009; Cancer progenitors and epigenetic contexts: an Xisting connection. Epigenetics 4:568–570 [View Article][PubMed]
     [Google Scholar]
  2. Agrelo R., Souabni A., Novatchkova M., Haslinger C., Leeb M., Komnenovic V., Kishimoto H., Gresh L., Kohwi-Shigematsu T., Kenner L. 2009; SATB1 defines the developmental context for gene silencing by Xist in lymphoma and embryonic cells. Dev Cell 16:507–516 [View Article][PubMed]
     [Google Scholar]
  3. Alvarez J. D., Yasui D. H., Niida H., Joh T., Loh D. Y., Kohwi-Shigematsu T. 2000; The MAR-binding protein SATB1 orchestrates temporal and spatial expression of multiple genes during T-cell development. Genes Dev 14:521–535[PubMed]
     [Google Scholar]
  4. Arbach H., Viglasky V., Lefeu F., Guinebretière J. M., Ramirez V., Bride N., Boualaga N., Bauchet T., Peyrat J. P. other authors 2006; Epstein–Barr virus (EBV) genome and expression in breast cancer tissue: effect of EBV infection of breast cancer cells on resistance to paclitaxel (Taxol). J Virol 80:845–853 [View Article][PubMed]
     [Google Scholar]
  5. Bai M., Papoudou-Bai A., Kitsoulis P., Horianopoulos N., Kamina S., Agnantis N. J., Kanavaros P. 2005; Cell cycle and apoptosis deregulation in classical Hodgkin lymphomas. In Vivo 19:439–453[PubMed]
     [Google Scholar]
  6. Brinkmann M. M., Schulz T. F. 2006; Regulation of intracellular signalling by the terminal membrane proteins of members of the Gammaherpesvirinae . J Gen Virol 87:1047–1074 [View Article][PubMed]
     [Google Scholar]
  7. Burgos J. S. 2005; Involvement of the Epstein–Barr virus in the nasopharyngeal carcinoma pathogenesis. Med Oncol 22:113–122 [View Article][PubMed]
     [Google Scholar]
  8. Cai S., Han H. J., Kohwi-Shigematsu T. 2003; Tissue-specific nuclear architecture and gene expression regulated by SATB1. Nat Genet 34:42–51 [View Article][PubMed]
     [Google Scholar]
  9. Cheng C., Lu X., Wang G., Zheng L., Shu X., Zhu S., Liu K., Wu K., Tong Q. 2010; Expression of SATB1 and heparanase in gastric cancer and its relationship to clinicopathologic features. APMIS 118:855–863 [View Article][PubMed]
     [Google Scholar]
  10. Cheung C. H., Cheng L., Chang K. Y., Chen H. H., Chang J. Y. 2011; Investigations of survivin: the past, present and future. Front Biosci 16:952–961 [View Article][PubMed]
     [Google Scholar]
  11. Church D. N., Talbot D. C. 2012; Survivin in solid tumors: rationale for development of inhibitors. Curr Oncol Rep 14:120–128 [View Article][PubMed]
     [Google Scholar]
  12. Contreras-Brodin B. A., Anvret M., Imreh S., Altiok E., Klein G., Masucci M. G. 1991; B cell phenotype-dependent expression of the Epstein-Barr virus nuclear antigens EBNA-2 to EBNA-6: studies with somatic cell hybrids. J Gen Virol 72:3025–3033 [View Article][PubMed]
     [Google Scholar]
  13. Dickinson L. A., Joh T., Kohwi Y., Kohwi-Shigematsu T. 1992; A tissue-specific MAR/SAR DNA-binding protein with unusual binding site recognition. Cell 70:631–645 [View Article][PubMed]
     [Google Scholar]
  14. Fukayama M., Hino R., Uozaki H. 2008; Epstein–Barr virus and gastric carcinoma: virus-host interactions leading to carcinoma. Cancer Sci 99:1726–1733 [View Article][PubMed]
     [Google Scholar]
  15. Han H. J., Russo J., Kohwi Y., Kohwi-Shigematsu T. 2008; SATB1 reprogrammes gene expression to promote breast tumour growth and metastasis. Nature 452:187–193 [View Article][PubMed]
     [Google Scholar]
  16. Hatzivassiliou E., Mosialos G. 2002; Cellular signaling pathways engaged by the Epstein–Barr virus transforming protein LMP1. Front Biosci 7:d319–d329 [View Article][PubMed]
     [Google Scholar]
  17. Hino R., Uozaki H., Inoue Y., Shintani Y., Ushiku T., Sakatani T., Takada K., Fukayama M. 2008; Survival advantage of EBV-associated gastric carcinoma: survivin up-regulation by viral latent membrane protein 2A. Cancer Res 68:1427–1435 [View Article][PubMed]
     [Google Scholar]
  18. Horikawa T., Yang J., Kondo S., Yoshizaki T., Joab I., Furukawa M., Pagano J. S. 2007; Twist and epithelial-mesenchymal transition are induced by the EBV oncoprotein latent membrane protein 1 and are associated with metastatic nasopharyngeal carcinoma. Cancer Res 67:1970–1978 [View Article][PubMed]
     [Google Scholar]
  19. Horikawa T., Yoshizaki T., Kondo S., Furukawa M., Kaizaki Y., Pagano J. S. 2011; Epstein–Barr virus latent membrane protein 1 induces Snail and epithelial-mesenchymal transition in metastatic nasopharyngeal carcinoma. Br J Cancer 104:1160–1167 [View Article][PubMed]
     [Google Scholar]
  20. Iorns E., Hnatyszyn H. J., Seo P., Clarke J., Ward T., Lippman M. 2010; The role of SATB1 in breast cancer pathogenesis. J Natl Cancer Inst 102:1284–1296 [View Article][PubMed]
     [Google Scholar]
  21. Izumi K. M. 2004; Epstein–Barr virus signal transduction and B-lymphocyte growth transformation. Prog Mol Subcell Biol 36:269–288[PubMed]
     [Google Scholar]
  22. Kanwar R. K., Cheung C. H., Chang J.-Y., Kanwar J. R. 2010; Recent advances in anti-survivin treatments for cancer. Curr Med Chem 17:1509–1515 [View Article][PubMed]
     [Google Scholar]
  23. Kanwar J. R., Kamalapuram S. K., Kanwar R. K. 2011; Targeting survivin in cancer: the cell-signalling perspective. Drug Discov Today 16:485–494 [View Article][PubMed]
     [Google Scholar]
  24. Kondo S., Wakisaka N., Schell M. J., Horikawa T., Sheen T. S., Sato H., Furukawa M., Pagano J. S., Yoshizaki T. 2005; Epstein–Barr virus latent membrane protein 1 induces the matrix metalloproteinase-1 promoter via an Ets binding site formed by a single nucleotide polymorphism: enhanced susceptibility to nasopharyngeal carcinoma. Int J Cancer 115:368–376 [View Article][PubMed]
     [Google Scholar]
  25. Kondo S., Seo S. Y., Yoshizaki T., Wakisaka N., Furukawa M., Joab I., Jang K. L., Pagano J. S. 2006; 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 66:9870–9877 [View Article][PubMed]
     [Google Scholar]
  26. Kondo S., Yoshizaki T., Wakisaka N., Horikawa T., Murono S., Jang K. L., Joab I., Furukawa M., Pagano J. S. 2007; MUC1 induced by Epstein–Barr virus latent membrane protein 1 causes dissociation of the cell-matrix interaction and cellular invasiveness via STAT signaling. J Virol 81:1554–1562 [View Article][PubMed]
     [Google Scholar]
  27. Kondo S., Wakisaka N., Muramatsu M., Zen Y., Endo K., Murono S., Sugimoto H., Yamaoka S., Pagano J. S., Yoshizaki T. 2011; Epstein–Barr virus latent membrane protein 1 induces cancer stem/progenitor-like cells in nasopharyngeal epithelial cell lines. J Virol 85:11255–11264 [View Article][PubMed]
     [Google Scholar]
  28. Kumar P. P., Purbey P. K., Ravi D. S., Mitra D., Galande S. 2005; Displacement of SATB1-bound histone deacetylase 1 corepressor by the human immunodeficiency virus type 1 transactivator induces expression of interleukin-2 and its receptor in T cells. Mol Cell Biol 25:1620–1633 [View Article][PubMed]
     [Google Scholar]
  29. Kumar P. P., Bischof O., Purbey P. K., Notani D., Urlaub H., Dejean A., Galande S. 2007; Functional interaction between PML and SATB1 regulates chromatin-loop architecture and transcription of the MHC class I locus. Nat Cell Biol 9:45–56 [View Article][PubMed]
     [Google Scholar]
  30. Kuo T. C., Chao C. C. 2010; Hepatitis B virus X protein prevents apoptosis of hepatocellular carcinoma cells by upregulating SATB1 and HURP expression. Biochem Pharmacol 80:1093–1102 [View Article][PubMed]
     [Google Scholar]
  31. Lam N., Sugden B. 2003; CD40 and its viral mimic, LMP1: similar means to different ends. Cell Signal 15:9–16 [View Article][PubMed]
     [Google Scholar]
  32. Li H. P., Chang Y. S. 2003; Epstein–Barr virus latent membrane protein 1: structure and functions. J Biomed Sci 10:490–504 [View Article][PubMed]
     [Google Scholar]
  33. Li K., Cai R., Dai B. B., Zhang X. Q., Wang H. J., Ge S. F., Xu W. R., Lu J. 2007; SATB1 regulates SPARC expression in K562 cell line through binding to a specific sequence in the third intron. Biochem Biophys Res Commun 356:6–12 [View Article][PubMed]
     [Google Scholar]
  34. Lippert B. M., Knauer S. K., Fetz V., Mann W., Stauber R. H. 2007; Dynamic survivin in head and neck cancer: molecular mechanism and therapeutic potential. Int J Cancer 121:1169–1174 [View Article][PubMed]
     [Google Scholar]
  35. Lladser A., Sanhueza C., Kiessling R., Quest A. F. 2011; Is survivin the potential Achilles’ heel of cancer?. Adv Cancer Res 111:1–37 [View Article][PubMed]
     [Google Scholar]
  36. Lo A. K., Liu Y., Wang X. H., Huang D. P., Yuen P. W., Wong Y. C., Tsao G. S. 2003; Alterations of biologic properties and gene expression in nasopharyngeal epithelial cells by the Epstein–Barr virus-encoded latent membrane protein 1. Lab Invest 83:697–709[PubMed] [CrossRef]
     [Google Scholar]
  37. Lu X., Cheng C., Zhu S., Yang Y., Zheng L., Wang G., Shu X., Wu K., Liu K., Tong Q. 2010; SATB1 is an independent prognostic marker for gastric cancer in a Chinese population. Oncol Rep 24:981–987[PubMed]
     [Google Scholar]
  38. Lu J., Murakami M., Verma S. C., Cai Q., Haldar S., Kaul R., Wasik M. A., Middeldorp J., Robertson E. S. 2011; Epstein–Barr virus nuclear antigen 1 (EBNA1) confers resistance to apoptosis in EBV-positive B-lymphoma cells through up-regulation of survivin. Virology 410:64–75 [View Article][PubMed]
     [Google Scholar]
  39. Mainou B. A., Everly D. N. Jr, Raab-Traub N. 2007; Unique signaling properties of CTAR1 in LMP1-mediated transformation. J Virol 81:9680–9692 [View Article][PubMed]
     [Google Scholar]
  40. Margulis V., Lotan Y., Shariat S. F. 2008; Survivin: a promising biomarker for detection and prognosis of bladder cancer. World J Urol 26:59–65 [View Article][PubMed]
     [Google Scholar]
  41. Marquitz A. R., Raab-Traub N. 2012; The role of miRNAs and EBV BARTs in NPC. Semin Cancer Biol 22:166–172 [View Article][PubMed]
     [Google Scholar]
  42. McGuire B. B., Fitzpatrick J. M. 2009; Biomarkers in renal cell carcinoma. Curr Opin Urol 19:441–446 [View Article][PubMed]
     [Google Scholar]
  43. Meng W. J., Yan H., Zhou B., Zhang W., Kong X. H., Wang R., Zhan L., Li Y., Zhou Z. G., Sun X. F. 2012; Correlation of SATB1 overexpression with the progression of human rectal cancer. Int J Colorectal Dis 27:143–150 [View Article][PubMed]
     [Google Scholar]
  44. Mori F., Piro F. R., Della Rocca C., Mesiti G., Giampaoli S., Silvestre G., Lazzaro D. 2007; Survivin and Cyclooxygenase-2 are co-expressed in human and mouse colon carcinoma and in terminally differentiated colonocytes. Histol Histopathol 22:61–77[PubMed]
     [Google Scholar]
  45. Morris M. A., Dawson C. W., Young L. S. 2009; Role of the Epstein–Barr virus-encoded latent membrane protein-1, LMP1, in the pathogenesis of nasopharyngeal carcinoma. Future Oncol 5:811–825 [View Article][PubMed]
     [Google Scholar]
  46. Murono S., Inoue H., Tanabe T., Joab I., Yoshizaki T., Furukawa M., Pagano J. S. 2001; Induction of cyclooxygenase-2 by Epstein–Barr virus latent membrane protein 1 is involved in vascular endothelial growth factor production in nasopharyngeal carcinoma cells. Proc Natl Acad Sci U S A 98:6905–6910 [View Article][PubMed]
     [Google Scholar]
  47. Pagano J. 2009 EBV Diseases In DNA Tumor Viruses pp 217–240 New York: Springer;
     [Google Scholar]
  48. Patani N., Jiang W., Mansel R., Newbold R., Mokbel K. 2009; The mRNA expression of SATB1 and SATB2 in human breast cancer. Cancer Cell Int 9:18 [View Article][PubMed]
     [Google Scholar]
  49. Pavan Kumar P., Purbey P. K., Sinha C. K., Notani D., Limaye A., Jayani R. S., Galande S. 2006; Phosphorylation of SATB1, a global gene regulator, acts as a molecular switch regulating its transcriptional activity in vivo. Mol Cell 22:231–243 [View Article][PubMed]
     [Google Scholar]
  50. Paydas S., Ergin M., Seydaoglu G., Erdogan S., Yavuz S. 2009; Prognostic [corrected] significance of angiogenic/lymphangiogenic, anti-apoptotic, inflammatory and viral factors in 88 cases with diffuse large B cell lymphoma and review of the literature. Leuk Res 33:1627–1635 [View Article][PubMed]
     [Google Scholar]
  51. Peng Z. K., Yang D. H., Li X. H., Huang Y., Zhang G. Q., Zhong K. B., Bi M. P., Li G. H. 2011; [Expression of special AT-rich sequence-binding protein 1 mRNA in hepatocellular carcinoma and its clinical significance]. Nan Fang Yi Ke Da Xue Xue Bao 31:1207–1211 (in Chinese) [PubMed]
     [Google Scholar]
  52. Savarese F., Dávila A., Nechanitzky R., De La Rosa-Velazquez I., Pereira C. F., Engelke R., Takahashi K., Jenuwein T., Kohwi-Shigematsu T. other authors 2009; Satb1 and Satb2 regulate embryonic stem cell differentiation and Nanog expression. Genes Dev 23:2625–2638 [View Article][PubMed]
     [Google Scholar]
  53. Shi W., Bastianutto C., Li A., Perez-Ordonez B., Ng R., Chow K. Y., Zhang W., Jurisica I., Lo K. W. other authors 2006; Multiple dysregulated pathways in nasopharyngeal carcinoma revealed by gene expression profiling. Int J Cancer 119:2467–2475 [View Article][PubMed]
     [Google Scholar]
  54. Shushan S., Cinamon U., Levy D., Sokolov M., Roth Y. 2009; Laryngeal cancer in acquired immunodeficiency syndrome. Int J STD AIDS 20:582–584 [View Article][PubMed]
     [Google Scholar]
  55. Slovin S. F., Glassy M. C., Dambaugh T., Catalano M. A., Curry R. A., Ferrone S., Kieff E., Vaughan J. H., Carson D. A. 1981; Discordant expression of 2 Epstein–Barr virus-associated antigens, EBNA and RANA, in man-rodent somatic cell hybrids. J Immunol 127:585–590[PubMed]
     [Google Scholar]
  56. Soni V., Cahir-McFarland E., Kieff E. 2007; LMP1 TRAFficking activates growth and survival pathways. Adv Exp Med Biol 597:173–187 [View Article][PubMed]
     [Google Scholar]
  57. Sun Y., Wang T., Su Y., Yin Y., Xu S., Ma C., Han X. 2006; The behavior of SATB1, a MAR-binding protein, in response to apoptosis stimulation. Cell Biol Int 30:244–247 [View Article][PubMed]
     [Google Scholar]
  58. Takimoto T., Sato H., Ogura H., Tanaka S., Umeda R. 1988; The difference in tumorigenicity between Epstein–Barr virus (EBV) genome-positive and genome-negative epithelial hybrid cell lines derived from the human nasopharynx. Laryngoscope 98:1334–1338 [View Article][PubMed]
     [Google Scholar]
  59. Tsao S. W., Tramoutanis G., Dawson C. W., Lo A. K., Huang D. P. 2002a; The significance of LMP1 expression in nasopharyngeal carcinoma. Semin Cancer Biol 12:473–487 [View Article][PubMed]
     [Google Scholar]
  60. Tsao S. W., Wang X., Liu Y., Cheung Y. C., Feng H., Zheng Z., Wong N., Yuen P. W., Lo A. K. other authors 2002b; Establishment of two immortalized nasopharyngeal epithelial cell lines using SV40 large T and HPV16E6/E7 viral oncogenes. Biochim Biophys Acta 1590:150–158 [View Article][PubMed]
     [Google Scholar]
  61. Tu W., Luo M., Wang Z., Yan W., Xia Y., Deng H., He J., Han P., Tian D. 2012; Upregulation of SATB1 promotes tumor growth and metastasis in liver cancer. Liver Int 32:1064–1078 [View Article][PubMed]
     [Google Scholar]
  62. Wakisaka N., Pagano J. S. 2003; Epstein–Barr virus induces invasion and metastasis factors. Anticancer Res 23:3A2133–2138[PubMed]
     [Google Scholar]
  63. Wakisaka N., Murono S., Yoshizaki T., Furukawa M., Pagano J. S. 2002; Epstein–Barr virus latent membrane protein 1 induces and causes release of fibroblast growth factor-2. Cancer Res 62:6337–6344[PubMed]
     [Google Scholar]
  64. Wakisaka N., Kondo S., Yoshizaki T., Murono S., Furukawa M., Pagano J. S. 2004; Epstein–Barr virus latent membrane protein 1 induces synthesis of hypoxia-inducible factor 1 alpha. Mol Cell Biol 24:5223–5234 [View Article][PubMed]
     [Google Scholar]
  65. Wen J., Huang S., Rogers H., Dickinson L. A., Kohwi-Shigematsu T., Noguchi C. T. 2005; SATB1 family protein expressed during early erythroid differentiation modifies globin gene expression. Blood 105:3330–3339 [View Article][PubMed]
     [Google Scholar]
  66. Yasui D., Miyano M., Cai S., Varga-Weisz P., Kohwi-Shigematsu T. 2002; SATB1 targets chromatin remodelling to regulate genes over long distances. Nature 419:641–645 [View Article][PubMed]
     [Google Scholar]
  67. Yoshizaki T., Sato H., Furukawa M., Pagano J. S. 1998; The expression of matrix metalloproteinase 9 is enhanced by Epstein–Barr virus latent membrane protein 1. Proc Natl Acad Sci U S A 95:3621–3626 [View Article][PubMed]
     [Google Scholar]
  68. Yoshizaki T., Wakisaka N., Pagano J. S. 2005 Epstein–Barr virus: Invasion and Metastasis Norfolk, UK: Caister Academic Press;
     [Google Scholar]
  69. Zhang Q., Zhang Z., Wang C., Xiao Z., Yu Y., Yang F., Chen Z., He Z. 2008a; Proteome analysis of the transformation potential of the Epstein–Barr virus-encoded latent membrane protein 1 in nasopharyngeal epithelial cells NP69. Mol Cell Biochem 314:73–83 [View Article][PubMed]
     [Google Scholar]
  70. Zhang R., Wang T., Li K. N., Qin W. W., Chen R., Wang K., Jia L. T., Zhao J., Wen W. H. other authors 2008b; A survivin double point mutant has potent inhibitory effect on the growth of hepatocellular cancer cells. Cancer Biol Ther 7:547–554 [View Article][PubMed]
     [Google Scholar]
  71. Zhao X. D., Ji W. Y., Zhang W., He L. X., Yang J., Liang H. J., Wang L. L. 2010; Overexpression of SATB1 in laryngeal squamous cell carcinoma. ORL J Otorhinolaryngol Relat Spec 72:1–5 [View Article][PubMed]
     [Google Scholar]
  72. Zheng J. 2008; Is SATB1 a master regulator in breast cancer growth and metastasis?. Womens Health (Lond Engl) 4:329–332 [View Article][PubMed]
     [Google Scholar]
  73. Zheng H., Li L. L., Hu D. S., Deng X. Y., Cao Y. 2007; Role of Epstein–Barr virus encoded latent membrane protein 1 in the carcinogenesis of nasopharyngeal carcinoma. Cell Mol Immunol 4:185–196[PubMed]
     [Google Scholar]
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Upregulation of special AT-rich-binding protein 1 by Epstein–Barr virus latent membrane protein 1 in human nasopharyngeal cells and nasopharyngeal cancer
J. Gen. Virol. 94, 507 (2013); https://doi.org/10.1099/vir.0.046243-0
/content/journal/jgv/10.1099/vir.0.046243-0
/content/journal/jgv/10.1099/vir.0.046243-0
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