Host-tumor interactions in nasopharyngeal carcinomas

Seminars in Cancer Biology

Volumn 22, Issue 2, 2012, Pages 127-136

  Gourzones, Claire ^a   Barjon, Clément ^a   Busson, Pierre ^a  

^a INSTITUT GUSTAVE ROUSSY   (France)

Author keywords

Exosomes; Metastatic niche; Plasma DNA and RNA; Regulatory T cells; Tumor infiltrating leucocytes

Indexed keywords

CHEMOKINE RECEPTOR CXCR; GAMMA INTERFERON INDUCIBLE PROTEIN 10; LATENT MEMBRANE PROTEIN 1; LATENT MEMBRANE PROTEIN 2;

CANCER IMMUNOLOGY; CD25+ T LYMPHOCYTE; CD3+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL EXPANSION; CELL HETEROGENEITY; CELL INFILTRATION; CELLULAR IMMUNITY; CYTOKINE PRODUCTION; DENDRITIC CELL; EPITHELIUM CELL; FIBROBLAST; GENE PRODUCT; HUMAN; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNOGENICITY; LEUKOCYTE; LYMPHOCYTE DIFFERENTIATION; NASOPHARYNX CARCINOMA; NATURAL KILLER CELL; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY T LYMPHOCYTE; REVIEW; T LYMPHOCYTE;

CHEMOKINE CCL20; CYTOKINES; EPSTEIN-BARR VIRUS INFECTIONS; EXOSOMES; HERPESVIRUS 4, HUMAN; HUMANS; MODELS, IMMUNOLOGICAL; NASOPHARYNGEAL NEOPLASMS; T-LYMPHOCYTES; TUMOR MICROENVIRONMENT;

EID: 84857787153     PISSN: 1044579X     EISSN: 10963650     Source Type: Journal    
DOI: 10.1016/j.semcancer.2012.01.002     Document Type: Review

References (142)

1. Sonnenschein C., Soto A.M. The death of the cancer cell. Cancer Res 2011, 71:4334-4337.
2. Schreiber R.D., Old L.J., Smyth M.J. Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion. Science 2011, 331:1565-1570.
3. Hanahan D., Weinberg R.A. Hallmarks of cancer: the next generation. Cell 2011, 144:646-674.
4. Fridman W.H., Galon J., Pages F., Tartour E., Sautes-Fridman C., Kroemer G. Prognostic and predictive impact of intra- and peritumoral immune infiltrates. Cancer Res 2011, 71:5601-5605.
5. Zitvogel L., Kepp O., Senovilla L., Menger L., Chaput N., Kroemer G. Immunogenic tumor cell death for optimal anticancer therapy: the calreticulin exposure pathway. Clin Cancer Res 2010, 16:3100-3104.
6. Redon C.E., Dickey J.S., Nakamura A.J., Kareva I.G., Naf D., Nowsheen S., et al. Tumors induce complex DNA damage in distant proliferative tissues in vivo. Proc Natl Acad Sci USA 2010, 107:17992-17997.
7. Critchley-Thorne R.J., Simons D.L., Yan N., Miyahira A.K., Dirbas F.M., Johnson D.L., et al. Impaired interferon signaling is a common immune defect in human cancer. Proc Natl Acad Sci USA 2009, 106:9010-9015.
8. Godtfredsen E. On the histopathology of malignant nasopharyngeal tumours. Acta Path Microbiol Scand Supp 1944, 55:38-319.
9. Klein G., Giovanella B.C., Lindahl T., Fialkow P.J., Singh S., Stehlin J.S. Direct evidence for the presence of Epstein-Barr virus DNA and nuclear antigen in malignant epithelial cells from patients with poorly differentiated carcinoma of the nasopharynx. Proc Natl Acad Sci USA 1974, 71:4737-4741.
10. Busson P., Ganem G., Flores P., Mugneret F., Clausse B., Caillou B., et al. Establishment and characterization of three transplantable EBV-containing nasopharyngeal carcinomas. Int J Cancer 1988, 42:599-606.
11. Nicholls J, Niedobitek G. Histopathological diagnosis of nasopharyngeal carcinoma - looking beyond the blue book. In: Busson P, editor. Nasopharyngeal carcinoma: from basic sciences to clinical management; 2008.
12. Teoh T. Epidermoid carcinoma of the nasopharynx among Chinese: a study of 31 necropsies. J Pathol Bacteriol 1957, 73:451-465.
13. Perry M., Whyte A. Immunology of the tonsils. Immunol Today 1998, 19:414-421.
14. Khabir A., Karray H., Rodriguez S., Rose M., Daoud J., Frikha M., et al. EBV latent membrane protein 1 abundance correlates with patient age but not with metastatic behavior in north African nasopharyngeal carcinomas. Virol J 2005, 2:39.
15. Cochet C., Martel-Renoir D., Grunewald V., Bosq J., Cochet G., Schwaab G., et al. Expression of the Epstein-Barr virus immediate early gene, BZLF1, in nasopharyngeal carcinoma tumor cells. Virology 1993, 197:358-365.
16. Sbih-Lammali F., Berger F., Busson P., Ooka T. Expression of the DNase encoded by the BGLF5 gene of Epstein-Barr virus in nasopharyngeal carcinoma epithelial cells. Virology 1996, 222:64-74.
17. Zhang J.X., Chen H.L., Zong Y.S., Chan K.H., Nicholls J., Middeldorp J.M., et al. Epstein-Barr virus expression within keratinizing nasopharyngeal carcinoma. J Med Virol 1998, 55:227-233.
18. Lee C.H., Yeh T.H., Lai H.C., Wu S.Y., Su I.J., Takada K., et al. Epstein-Barr virus Zta-induced immunomodulators from nasopharyngeal carcinoma cells upregulate interleukin-10 production from monocytes. J Virol 2011, 85:7333-7342.
19. Hsu M., Wu S.Y., Chang S.S., Su I.J., Tsai C.H., Lai S.J., et al. Epstein-Barr virus lytic transactivator Zta enhances chemotactic activity through induction of interleukin-8 in nasopharyngeal carcinoma cells. J Virol 2008, 82:3679-3688.
20. Henle G., Henle W., Serum IgA antibodies of Epstein-Barr virus (EBV)-related antigens. A new feature of nasopharyngeal carcinoma. Bibliotheca Haematol 1975, 322-325.
21. Chien Y.C., Chen J.Y., Liu M.Y., Yang H.I., Hsu M.M., Chen C.J., et al. Serologic markers of Epstein-Barr virus infection and nasopharyngeal carcinoma in Taiwanese men. N Engl J Med 2001, 345:1877-1882.
22. Herait P., Ganem G., Lipinski M., Carlu C., Micheau C., Schwaab G., et al. Lymphocyte subsets in tumour of patients with undifferentiated nasopharyngeal carcinoma: presence of lymphocytes with the phenotype of activated T cells. Br J Cancer 1987, 55:135-139.
23. Ferradini L., Miescher S., Stoeck M., Busson P., Barras C., Cerf-Bensussan N., et al. Cytotoxic potential despite impaired activation pathways in T lymphocytes infiltrating nasopharyngeal carcinoma. Int J Cancer 1991, 47:362-370.
24. Hu H., Tang K.F., Chua Y.N., Lu J., Feng P., Chew C.T., et al. Expression of interleukin-18 by nasopharyngeal carcinoma cells: a factor that possibly initiates the massive leukocyte infiltration. Hum Pathol 2004, 35:722-728.
25. Agathanggelou A., Niedobitek G., Chen R., Nicholls J., Yin W., Young L.S. Expression of immune regulatory molecules in Epstein-Barr virus-associated nasopharyngeal carcinomas with prominent lymphoid stroma Evidence for a functional interaction between epithelial tumor cells and infiltrating lymphoid cells. Am J Pathol 1995, 147:1152-1160.
26. Zong Y.S., Zhang C.Q., Zhang F., Ruan J.B., Chen M.Y., Feng K.T., et al. Infiltrating lymphocytes and accessory cells in nasopharyngeal carcinoma. Jpn J Cancer Res 1993, 84:900-905.
27. Giannini A., Bianchi S., Messerini L., Gallo O., Gallina E., Asprella Libonati G., et al. Prognostic significance of accessory cells and lymphocytes in nasopharyngeal carcinoma. Pathol Res Pract 1991, 187:496-502.
28. Ma C.X., Jia T.C., Li X.R., Zhand Z.F., Yiao C.B. Langerhans cells in nasopharyngeal carcinoma in relation to prognosis. In Vivo 1995, 9:225-229.
29. Tang K.F., Tan S.Y., Chan S.H., Chong S.M., Loh K.S., Tan L.K., et al. A distinct expression of CC chemokines by macrophages in nasopharyngeal carcinoma: implication for the intense tumor infiltration by T lymphocytes and macrophages. Hum Pathol 2001, 32:42-49.
30. Niedobitek G., Young L.S., Sam C.K., Brooks L., Prasad U., Rickinson A.B. Expression of Epstein-Barr virus genes and of lymphocyte activation molecules in undifferentiated nasopharyngeal carcinomas. Am J Pathol 1992, 140:879-887.
31. Leighton S.E., Teo J.G., Leung S.F., Cheung A.Y., Lee J.C., van Hasselt C.A. Prevalence and prognostic significance of tumor-associated tissue eosinophilia in nasopharyngeal carcinoma. Cancer 1996, 77:436-440.
32. Liu C.M., Ko J.J., Shun C.T., Hsiao T.Y., Sheen T.S. Soluble adhesion molecules and cytokines in tumor-associated tissue eosinophilia of nasopharyngeal carcinoma. Acta Otolaryngol 2001, 121:534-538.
33. Lau K.M., Cheng S.H., Lo K.W., Lee S.A., Woo J.K., van Hasselt C.A., et al. Increase in circulating Foxp3+CD4+CD25(high) regulatory T cells in nasopharyngeal carcinoma patients. Br J Cancer 2007, 96:617-622.
34. Yip W.K., Abdullah M.A., Yusoff S.M., Seow H.F. Increase in tumour-infiltrating lymphocytes with regulatory T cell immunophenotypes and reduced zeta-chain expression in nasopharyngeal carcinoma patients. Clin Exp Immunol 2009, 155:412-422.
35. Teichmann M., Meyer B., Beck A., Niedobitek G. Expression of the interferon-inducible chemokine IP-10 (CXCL10), a chemokine with proposed anti-neoplastic functions, in Hodgkin lymphoma and nasopharyngeal carcinoma. J Pathol 2005, 206:68-75.
36. Zhang Y.L., Li J., Mo H.Y., Qiu F., Zheng L.M., Qian C.N., et al. Different subsets of tumor infiltrating lymphocytes correlate with NPC progression in different ways. Mol Cancer 2010, 9:4.
37. Li J., Huang Z.F., Xiong G., Mo H.Y., Qiu F., Mai H.Q., et al. Distribution, characterization, and induction of CD8+ regulatory T cells and IL-17-producing CD8+ T cells in nasopharyngeal carcinoma. J Transl Med 2011, 9:189.
38. Kim H.J., Wang X., Radfar S., Sproule T.J., Roopenian D.C., Cantor H. CD8+ T regulatory cells express the Ly49 Class I MHC receptor and are defective in autoimmune prone B6-Yaa mice. Proc Natl Acad Sci USA 2011, 108:2010-2015.
39. Braham H., Trimeche M., Ziadi S., Mestiri S., Mokni M., Amara K., et al. CD10 expression by fusiform stromal cells in nasopharyngeal carcinoma correlates with tumor progression. Virchows Arch 2006, 449:220-224.
40. Hui E.P., Chan A.T., Pezzella F., Turley H., To K.F., Poon T.C., et al. Coexpression of hypoxia-inducible factors 1alpha and 2alpha, carbonic anhydrase IX, and vascular endothelial growth factor in nasopharyngeal carcinoma and relationship to survival. Clin Cancer Res 2002, 8:2595-2604.
41. Ma B.B., Poon T.C., To K.F., Zee B., Mo F.K., Chan C.M., et al. Prognostic significance of tumor angiogenesis, Ki 67, p53 oncoprotein, epidermal growth factor receptor and HER2 receptor protein expression in undifferentiated nasopharyngeal carcinoma--a prospective study. Head Neck 2003, 25:864-872.
42. Rubio L., Burgos J.S., Morera C., Vera-Sempere F.J. Morphometric study of tumor angiogenesis as a new prognostic factor in nasopharyngeal carcinoma patients. Pathol Oncol Res 2000, 6:210-216.
43. Busson P., Braham K., Ganem G., Thomas F., Grausz D., Lipinski M., et al. Epstein-Barr virus-containing epithelial cells from nasopharyngeal carcinoma produce interleukin 1 alpha. Proc Natl Acad Sci USA 1987, 84:6262-6266.
44. Huang Y.T., Sheen T.S., Chen C.L., Lu J., Chang Y., Chen J.Y., et al. Profile of cytokine expression in nasopharyngeal carcinomas: a distinct expression of interleukin 1 in tumor and CD4+ T cells. Cancer Res 1999, 59:1599-1605.
45. Beck A., Pazolt D., Grabenbauer G.G., Nicholls J.M., Herbst H., Young L.S., et al. Expression of cytokine and chemokine genes in Epstein-Barr virus-associated nasopharyngeal carcinoma: comparison with Hodgkin's disease. J Pathol 2001, 194:145-151.
46. Chang K.P., Hao S.P., Chang J.H., Wu C.C., Tsang N.M., Lee Y.S., et al. Macrophage inflammatory protein-3alpha is a novel serum marker for nasopharyngeal carcinoma detection and prediction of treatment outcomes. Clin Cancer Res 2008, 14:6979-6987.
47. Baumforth K.R., Birgersdotter A., Reynolds G.M., Wei W., Kapatai G., Flavell J.R., et al. Expression of the Epstein-Barr virus-encoded Epstein-Barr virus nuclear antigen 1 in Hodgkin's lymphoma cells mediates up-regulation of CCL20 and the migration of regulatory T cells. Am J Pathol 2008, 173:195-204.
48. Tang K.F., Chan S.H., Loh K.S., Chong S.M., Wang D., Yeoh K.H., et al. Increased production of interferon-gamma by tumour infiltrating T lymphocytes in nasopharyngeal carcinoma: indicative of an activated status. Cancer Lett 1999, 140:93-98.
49. Li J., Zeng X.H., Mo H.Y., Rolen U., Gao Y.F., Zhang X.S., et al. Functional inactivation of EBV-specific T-lymphocytes in nasopharyngeal carcinoma: implications for tumor immunotherapy. PLoS One 2007, 2:e1122.
50. Nanbo A., Takada K. The role of Epstein-Barr virus-encoded small RNAs (EBERs) in oncogenesis. Rev Med Virol 2002, 12:321-326.
51. Shah K.M., Stewart S.E., Wei W., Woodman C.B., O'Neil J.D., Dawson C.W., et al. The EBV-encoded latent membrane proteins LMP2A and LMP2B, limit the actions of interferon by targeting interferon receptors for degradation. Oncogene 2009, 28:3903-3914.
52. Lee K.Y., Geng H., Ng K.M., Yu J., van Hasselt A., Cao Y., et al. Epigenetic disruption of interferon-gamma response through silencing the tumor suppressor interferon regulatory factor 8 in nasopharyngeal, esophageal and multiple other carcinomas. Oncogene 2008, 27:5267-5276.
53. Marangoni E., Vincent-Salomon A., Auger N., Degeorges A., Assayag F., de Cremoux P., et al. A new model of patient tumor-derived breast cancer xenografts for preclinical assays. Clin Cancer Res 2007, 13:3989-3998.
54. Caggiari L., Guidoboni M., Vaccher E., Barzan L., Franchin G., Gloghini A., et al. High serum levels of soluble CD40-L in patients with undifferentiated nasopharyngeal carcinoma: pathogenic and clinical relevance. Infect Agent Cancer 2007, 2:5.
55. Sbih-Lammali F., Clausse B., Ardila-Osorio H., Guerry R., Talbot M., Havouis S., et al. Control of apoptosis in Epstein-Barr virus-positive nasopharyngeal carcinoma cells: opposite effects of CD95 and CD40 stimulation. Cancer Res 1999, 59:924-930.
56. Benson R.J., Hostager B.S., Bishop G.A. Rapid CD40-mediated rescue from CD95-induced apoptosis requires TNFR-associated factor-6 and PI3K. Eur J Immunol 2006, 36:2535-2543.
57. Baxendale A.J., Dawson C.W., Stewart S.E., Mudaliar V., Reynolds G., Gordon J., et al. Constitutive activation of the CD40 pathway promotes cell transformation and neoplastic growth. Oncogene 2005, 24:7913-7923.
58. Qian C.N., Guo X., Cao B., Kort E.J., Lee C.C., Chen J., et al. Met protein expression level correlates with survival in patients with late-stage nasopharyngeal carcinoma. Cancer Res 2002, 62:589-596.
59. Naran S., Zhang X., Hughes S.J. Inhibition of HGF/MET as therapy for malignancy. Expert Opin Ther Targets 2009, 13:569-581.
60. Orimo A., Gupta P.B., Sgroi D.C., Arenzana-Seisdedos F., Delaunay T., Naeem R., et al. Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion. Cell 2005, 121:335-348.
61. Wang N., Wu Q.L., Fang Y., Mai H.Q., Zeng M.S., Shen G.P., et al. Expression of chemokine receptor CXCR4 in nasopharyngeal carcinoma: pattern of expression and correlation with clinical outcome. J Transl Med 2005, 3:26.
62. Sheu L.F., Lee W.C., Lee H.S., Kao W.Y., Chen A. Co-expression of c-kit and stem cell factor in primary and metastatic nasopharyngeal carcinomas and nasopharyngeal epithelium. J Pathol 2005, 207:216-223.
63. Samanta M., Iwakiri D., Kanda T., Imaizumi T., Takada K. EB virus-encoded RNAs are recognized by RIG-I and activate signaling to induce type I IFN. EMBO J 2006, 25:4207-4214.
64. Iwakiri D., Sheen T.S., Chen J.Y., Huang D.P., Takada K. Epstein-Barr virus-encoded small RNA induces insulin-like growth factor 1 and supports growth of nasopharyngeal carcinoma-derived cell lines. Oncogene 2005, 24:1767-1773.
65. Seto E., Yang L., Middeldorp J., Sheen T.S., Chen J.Y., Fukayama M., et al. Epstein-Barr virus (EBV)-encoded BARF1 gene is expressed in nasopharyngeal carcinoma and EBV-associated gastric carcinoma tissues in the absence of lytic gene expression. J Med Virol 2005, 76:82-88.
66. Sall A., Caserta S., Jolicoeur P., Franqueville L., de Turenne-Tessier M., Ooka T. Mitogenic activity of Epstein-Barr virus-encoded BARF1 protein. Oncogene 2004, 23:4938-4944.
67. Cvitkovic E., Bachouchi M., Boussen H., Busson P., Rousselet G., Mahjoubi R., et al. Leukemoid reaction, bone marrow invasion, fever of unknown origin, and metastatic pattern in the natural history of advanced undifferentiated carcinoma of nasopharyngeal type: a review of 255 consecutive cases. J Clin Oncol 1993, 11:2434-2442.
68. Pantel K., Alix-Panabieres C., Riethdorf S. Cancer micrometastases. Nat Rev Clin Oncol 2009, 6:339-351.
69. Malanchi I., Santamaria-Martinez A., Susanto E., Peng H., Lehr H.A., Delaloye J.F., et al. Interactions between cancer stem cells and their niche govern metastatic colonization. Nature 2011.
70. Psaila B., Lyden D. The metastatic niche: adapting the foreign soil. Nat Rev Cancer 2009, 9:285-293.
71. Stevens S.J., Verkuijlen S.A., Hariwiyanto B., Harijadi, Fachiroh J., Paramita D.K., et al. Diagnostic value of measuring Epstein-Barr virus (EBV) DNA load and carcinoma-specific viral mRNA in relation to anti-EBV immunoglobulin A (IgA) and IgG antibody levels in blood of nasopharyngeal carcinoma patients from Indonesia. J Clin Microbiol 2005, 43:3066-3073.
72. Peinado H., Lavotshkin S., Lyden D. The secreted factors responsible for pre-metastatic niche formation: old sayings and new thoughts. Semin Cancer Biol 2011, 21:139-146.
73. Wang H.Y., Sun B.Y., Zhu Z.H., Chang E.T., To K.F., Hwang J.S., et al. Eight-signature classifier for prediction of nasopharnyngeal carcinoma survival. J Clin Oncol 2011, 29:4516-4525.
74. Chang K.P., Chang Y.T., Wu C.C., Liu Y.L., Chen M.C., Tsang N.M., et al. Multiplexed immunobead-based profiling of cytokine markers for detection of nasopharyngeal carcinoma and prognosis of patient survival. Head Neck 2011, 33:886-897.
75. Li J., Chen Q.Y., Mo H., Zhang Y.L., Huang Z.F., Zeng Y.X. Immunophenotyping at the time of diagnosis distinguishes two groups of nasopharyngeal carcinoma patients: implications for adoptive immunotherapy. Int J Biol Sci 2011, 7:607-617.
76. He J.R., Qin H., Ren Z.F., Cui C., Zhang Y., Ranatunga D., et al. MMP-9 expression in peripheral blood mononuclear cells and the association with clinicopathological features and prognosis of nasopharyngeal carcinoma. Clin Chem Lab Med 2011, 49:705-710.
77. Zheng B.J., Ng S.P., Chua D.T., Sham J.S., Kwong D.L., Lam C.K., et al. Peripheral gamma delta T-cell deficit in nasopharyngeal carcinoma. Int J Cancer 2002, 99:213-217.
78. Rousselet G., Bachouchi M., Busson P., de Vathaire F., Wakasugi H., Schwaab G., et al. Clinical implications of the serum level of CD23 in patients with undifferentiated nasopharyngeal carcinoma. J Clin Oncol 1993, 11:2143-2149.
79. Xu J., Menezes J., Prasad U., Ahmad A. Elevated serum levels of transforming growth factor beta1 in Epstein-Barr virus-associated nasopharyngeal carcinoma patients. Int J Cancer 1999, 84:396-399.
80. Houali K., Wang X., Shimizu Y., Djennaoui D., Nicholls J., Fiorini S., et al. A new diagnostic marker for secreted Epstein-Barr virus encoded LMP1 and BARF1 oncoproteins in the serum and saliva of patients with nasopharyngeal carcinoma. Clin Cancer Res 2007, 13:4993-5000.
81. Chang K.P., Wu C.C., Chen H.C., Chen S.J., Peng P.H., Tsang N.M., et al. Identification of candidate nasopharyngeal carcinoma serum biomarkers by cancer cell secretome and tissue transcriptome analysis: potential usage of cystatin A for predicting nodal stage and poor prognosis. Proteomics 2010, 10:2644-2660.
82. Schorey J.S., Bhatnagar S. Exosome function: from tumor immunology to pathogen biology. Traffic 2008, 9:871-881.
83. Valadi H., Ekstrom K., Bossios A., Sjostrand M., Lee J.J., Lotvall J.O. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 2007, 9:654-659.
84. Lakkaraju A., Rodriguez-Boulan E. Itinerant exosomes: emerging roles in cell and tissue polarity. Trends Cell Biol 2008, 18:199-209.
85. Iero M., Valenti R., Huber V., Filipazzi P., Parmiani G., Fais S., et al. Tumour-released exosomes and their implications in cancer immunity. Cell Death Differ 2008, 15:80-88.
86. Klibi J., Niki T., Riedel A., Pioche-Durieu C., Souquere S., Rubinstein E., et al. Blood diffusion and Th1-suppressive effects of galectin-9-containing exosomes released by Epstein-Barr virus-infected nasopharyngeal carcinoma cells. Blood 2009, 113:1957-1966.
87. Zhu C., Anderson A.C., Schubart A., Xiong H., Imitola J., Khoury S.J., et al. The Tim-3 ligand galectin-9 negatively regulates T helper type 1 immunity. Nat Immunol 2005, 6:1245-1252.
88. Keryer-Bibens C., Pioche-Durieu C., Villemant C., Souquere S., Nishi N., Hirashima M., et al. Exosomes released by EBV-infected nasopharyngeal carcinoma cells convey the viral latent membrane protein 1 and the immunomodulatory protein galectin 9. BMC Cancer 2006, 6:283.
89. Meckes D.G., Shair K.H., Marquitz A.R., Kung C.P., Edwards R.H., Raab-Traub N. Human tumor virus utilizes exosomes for intercellular communication. Proc Natl Acad Sci USA 2010, 107:20370-20375.
90. Gourzones C., Gelin A., Bombik I., Klibi J., Verillaud B., Guigay J., et al. Extra-cellular release and blood diffusion of BART viral micro-RNAs produced by EBV-infected nasopharyngeal carcinoma cells. Virol J 2010, 7:271.
91. Wong AM, Kong KL, Tsang JW, Kwong DL, Guan XY. Profiling of Epstein-Barr virus-encoded microRNAs in nasopharyngeal carcinoma reveals potential biomarkers and oncomirs. Cancer. 2011.
92. Lin J.C., Wang W.Y., Chen K.Y., Wei Y.H., Liang W.M., Jan J.S., et al. Quantification of plasma Epstein-Barr virus DNA in patients with advanced nasopharyngeal carcinoma. N Engl J Med 2004, 350:2461-2470.
93. Lo K.W., Lo Y.M., Leung S.F., Tsang Y.S., Chan L.Y., Johnson P.J., et al. Analysis of cell-free Epstein-Barr virus associated RNA in the plasma of patients with nasopharyngeal carcinoma. Clin Chem 1999, 45:1292-1294.
94. Mutirangura A., Pornthanakasem W., Theamboonlers A., Sriuranpong V., Lertsanguansinchi P., Yenrudi S., et al. Epstein-Barr viral DNA in serum of patients with nasopharyngeal carcinoma. Clin Cancer Res 1998, 4:665-669.
95. Wong T.S., Kwong D.L., Sham J.S., Wei W.I., Kwong Y.L., Yuen A.P. Quantitative plasma hypermethylated DNA markers of undifferentiated nasopharyngeal carcinoma. Clin Cancer Res 2004, 10:2401-2406.
96. Jahr S., Hentze H., Englisch S., Hardt D., Fackelmayer F.O., Hesch R.D., et al. DNA fragments in the blood plasma of cancer patients: quantitations and evidence for their origin from apoptotic and necrotic cells. Cancer Res 2001, 61:1659-1665.
97. Chan K.C., Zhang J., Chan A.T., Lei K.I., Leung S.F., Chan L.Y., et al. Molecular characterization of circulating EBV DNA in the plasma of nasopharyngeal carcinoma and lymphoma patients. Cancer Res 2003, 63:2028-2032.
98. Vickers K.C., Palmisano B.T., Shoucri B.M., Shamburek R.D., Remaley A.T. MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat Cell Biol 2011, 13:423-433.
99. Arroyo J.D., Chevillet J.R., Kroh E.M., Ruf I.K., Pritchard C.C., Gibson D.F., et al. Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc Natl Acad Sci USA 2011, 108:5003-5008.
100. Pegtel D.M., Cosmopoulos K., Thorley-Lawson D.A., van Eijndhoven M.A., Hopmans E.S., Lindenberg J.L., et al. Functional delivery of viral miRNAs via exosomes. Proc Natl Acad Sci USA 2010, 107:6328-6333.
101. Chen D.Y., Chen Y.M., Lan J.L., Chen H.H., Hsieh C.W., Wey S.J., et al. Polymyositis/dermatomyositis and nasopharyngeal carcinoma: the Epstein-Barr virus connection?. J Clin Virol 2010, 49:290-295.
102. Huang Y.L., Chen Y.J., Lin M.W., Wu C.Y., Liu P.C., Chen T.J., et al. Malignancies associated with dermatomyositis and polymyositis in Taiwan: a nationwide population-based study. Br J Dermatol 2009, 161:854-860.
103. Jalbout M., Bel Hadj Jrad B., Bouaouina N., Gargouri J., Yacoub S., Zakhama A., et al. Autoantibodies to tubulin are specifically associated with the young age onset of the nasopharyngeal carcinoma. Int J Cancer 2002, 101:146-150.
104. Purgina B., Pantanowitz L., Seethala R.R. A review of carcinomas arising in the head and neck region in HIV-positive patients. Patholog Res Int 2011, 2011:469150.
105. Fachiroh J., Stevens S.J., Haryana S.M., Middeldorp J.M. Combination of Epstein-Barr virus scaffold (BdRF1/VCA-p40) and small capsid protein (BFRF3/VCA-p18) into a single molecule for improved serodiagnosis of acute and malignant EBV-driven disease. J Virol Methods 2010, 169:79-86.
106. Joab I., Nicolas J.C., Schwaab G., de-The G., Clausse B., Perricaudet M., et al. Detection of anti-Epstein-Barr-virus transactivator (ZEBRA) antibodies in sera from patients with nasopharyngeal carcinoma. Int J Cancer 1991, 48:647-649.
107. Xu J., Ahmad A., Blagdon M., D'Addario M., Jones J.F., Dolcetti R., et al. The Epstein-Barr virus (EBV) major envelope glycoprotein gp350/220-specific antibody reactivities in the sera of patients with different EBV-associated diseases. Int J Cancer 1998, 79:481-486.
108. Yu K.J., Hsu W.L., Pfeiffer R.M., Chiang C.J., Wang C.P., Lou P.J., et al. Prognostic utility of anti-EBV antibody testing for defining NPC risk among individuals from high-risk NPC families. Clin Cancer Res 2011, 17:1906-1914.
109. Xu J., Ahmad A., D'Addario M., Knafo L., Jones J.F., Prasad U., et al. Analysis and significance of anti-latent membrane protein-1 antibodies in the sera of patients with EBV-associated diseases. J Immunol 2000, 164:2815-2822.
110. Frech B., Zimber-Strobl U., Suentzenich K.O., Pavlish O., Lenoir G.M., Bornkamm G.W., et al. Identification of Epstein-Barr virus terminal protein 1 (TP1) in extracts of four lymphoid cell lines, expression in insect cells, and detection of antibodies in human sera. J Virol 1990, 64:2759-2767.
111. Paramita D.K., Fatmawati C., Juwana H., van Schaijk F.G., Fachiroh J., Haryana S.M., et al. Humoral immune responses to Epstein-Barr virus encoded tumor associated proteins and their putative extracellular domains in nasopharyngeal carcinoma patients and regional controls. J Med Virol 2011, 83:665-678.
112. Hoebe E.K., Hutajulu S.H., van Beek J., Stevens S.J., Paramita D.K., Greijer A.E., et al. Purified hexameric Epstein-Barr virus-encoded BARF1 protein for measuring anti-BARF1 antibody responses in nasopharyngeal carcinoma patients. Clin Vaccine Immunol 2011, 18:298-304.
113. Lin X., Gudgeon N.H., Hui E.P., Jia H., Qun X., Taylor G.S., et al. CD4 and CD8T cell responses to tumour-associated Epstein-Barr virus antigens in nasopharyngeal carcinoma patients. Cancer Immunol Immunother 2008, 57:963-975.
114. Martorelli D., Houali K., Caggiari L., Vaccher E., Barzan L., Franchin G., et al. Spontaneous T cell responses to Epstein-Barr virus-encoded BARF1 protein and derived peptides in patients with nasopharyngeal carcinoma: bases for improved immunotherapy. Int J Cancer 2008, 123:1100-1107.
115. Sengupta S., den Boon J.A., Chen I.H., Newton M.A., Dahl D.B., Chen M., et al. Genome-wide expression profiling reveals EBV-associated inhibition of MHC class I expression in nasopharyngeal carcinoma. Cancer Res 2006, 66:7999-8006.
116. Lee S.P., Chan A.T., Cheung S.T., Thomas W.A., CroomCarter D., Dawson C.W., et al. CTL control of EBV in nasopharyngeal carcinoma (NPC): EBV-specific CTL responses in the blood and tumors of NPC patients and the antigen-processing function of the tumor cells. J Immunol 2000, 165:573-582.
117. Khanna R., Busson P., Burrows S.R., Raffoux C., Moss D.J., Nicholls J.M., et al. Molecular characterization of antigen-processing function in nasopharyngeal carcinoma (NPC): evidence for efficient presentation of Epstein-Barr virus cytotoxic T-cell epitopes by NPC cells. Cancer Res 1998, 58:310-314.
118. Louis C.U., Straathof K., Bollard C.M., Ennamuri S., Gerken C., Lopez T.T., et al. Adoptive transfer of EBV-specific T cells results in sustained clinical responses in patients with locoregional nasopharyngeal carcinoma. J Immunother 2010, 33:983-990.
119. Zitvogel L., Tesniere A., Kroemer G. Cancer despite immunosurveillance: immunoselection and immunosubversion. Nat Rev Immunol 2006, 6:715-727.
120. Yao M., Ohshima K., Suzumiya J., Kume T., Shiroshita T., Kikuchi M. Interleukin-10 expression and cytotoxic-T-cell response in Epstein-Barr-virus-associated nasopharyngeal carcinoma. Int J Cancer 1997, 72:398-402.
121. Fujieda S., Lee K., Sunaga H., Tsuzuki H., Ikawa H., Fan G.K., et al. Staining of interleukin-10 predicts clinical outcome in patients with nasopharyngeal carcinoma. Cancer 1999, 85:1439-1445.
122. Ozyar E., Ayhan A., Korcum A.F., Atahan I.L. Prognostic role of Epstein-Barr virus latent membrane protein-1 and interleukin-10 expression in patients with nasopharyngeal carcinoma. Cancer Invest 2004, 22:483-491.
123. Xu J., Ahmad A., Jones J.F., Dolcetti R., Vaccher E., Prasad U., et al. Elevated serum transforming growth factor beta1 levels in Epstein-Barr virus-associated diseases and their correlation with virus-specific immunoglobulin A (IgA) and IgM. J Virol 2000, 74:2443-2446.
124. Ho S.Y., Guo H.R., Chen H.H., Hsiao J.R., Jin Y.T., Tsai S.T. Prognostic implications of Fas-ligand expression in nasopharyngeal carcinoma. Head Neck 2004, 26:977-983.
125. Hsu M.C., Hsiao J.R., Chang K.C., Wu Y.H., Su I.J., Jin Y.T., et al. Increase of programmed death-1-expressing intratumoral CD8T cells predicts a poor prognosis for nasopharyngeal carcinoma. Mod Pathol 2010, 23:1393-1403.
126. Tripathi P. Nitric oxide and immune response. Indian J Biochem Biophys 2007, 44:310-319.
127. Ma N., Kawanishi M., Hiraku Y., Murata M., Huang G.W., Huang Y., et al. Reactive nitrogen species-dependent DNA damage in EBV-associated nasopharyngeal carcinoma: the relation to STAT3 activation and EGFR expression. Int J Cancer 2008, 122:2517-2525.
128. Clayton A., Al-Taei S., Webber J., Mason M.D., Tabi Z. Cancer exosomes express CD39 and CD73, which suppress T cells through adenosine production. J Immunol 2011, 187:676-683.
129. Pioche-Durieu C., Keryer C., Souquere S., Bosq J., Faigle W., Loew D., et al. In nasopharyngeal carcinoma cells, Epstein-Barr virus LMP1 interacts with galectin 9 in membrane raft elements resistant to simvastatin. J Virol 2005, 79:13326-13337.
130. Reddy P.B., Sehrawat S., Suryawanshi A., Rajasagi N.K., Mulik S., Hirashima M., et al. Influence of galectin-9/tim-3 interaction on herpes simplex virus-1 latency. J Immunol 2011, 187:5745-5755.
131. Sharma S., Sundararajan A., Suryawanshi A., Kumar N., Veiga-Parga T., Kuchroo V.K., et al. T cell immunoglobulin and mucin protein-3 (Tim-3)/Galectin-9 interaction regulates influenza A virus-specific humoral and CD8 T-cell responses. Proc Natl Acad Sci USA 2011, 108:19001-19006.
132. Seki M., Oomizu S., Sakata K.M., Sakata A., Arikawa T., Watanabe K., et al. Galectin-9 suppresses the generation of Th17, promotes the induction of regulatory T cells, and regulates experimental autoimmune arthritis. Clin Immunol 2008, 127:78-88.
133. Dukers D.F., Meij P., Vervoort M.B., Vos W., Scheper R.J., Meijer C.J., et al. Direct immunosuppressive effects of EBV-encoded latent membrane protein 1. J Immunol 2000, 165:663-670.
134. Voo K.S., Peng G., Guo Z., Fu T., Li Y., Frappier L., et al. Functional characterization of EBV-encoded nuclear antigen 1-specific CD4+ helper and regulatory T cells elicited by in vitro peptide stimulation. Cancer Res 2005, 65:1577-1586.
135. Edwards R.H., Sitki-Green D., Moore D.T., Raab-Traub N. Potential selection of LMP1 variants in nasopharyngeal carcinoma. J Virol 2004, 78:868-881.
136. Oudejans J.J., Harijadi H., Kummer J.A., Tan I.B., Bloemena E., Middeldorp J.M., et al. High numbers of granzyme B/CD8-positive tumour-infiltrating lymphocytes in nasopharyngeal carcinoma biopsies predict rapid fatal outcome in patients treated with curative intent. J Pathol 2002, 198:468-475.
137. Fridman W.H., Galon J., Dieu-Nosjean M.C., Cremer I., Fisson S., Damotte D., et al. Immune infiltration in human cancer: prognostic significance and disease control. Curr Top Microbiol Immunol 2011, 344:1-24.
138. Chan K.H., Gu Y.L., Ng F., Ng P.S., Seto W.H., Sham J.S., et al. EBV specific antibody-based and DNA-based assays in serologic diagnosis of nasopharyngeal carcinoma. Int J Cancer 2003, 105:706-709.
139. Fan H., Nicholls J., Chua D., Chan K.H., Sham J., Lee S., et al. Laboratory markers of tumor burden in nasopharyngeal carcinoma: a comparison of viral load and serologic tests for Epstein-Barr virus. Int J Cancer 2004, 112:1036-1041.
140. Galon J., Fridman W.H., Pages F. The adaptive immunologic microenvironment in colorectal cancer: a novel perspective. Cancer Res 2007, 67:1883-1886.
141. Mantovani A., Germano G., Marchesi F., Locatelli M., Biswas S.K. Cancer-promoting tumor-associated macrophages: new vistas and open questions. Eur J Immunol 2011, 41:2522-2525.
142. Lipson E.J., Drake C.G. Ipilimumab an anti-CTLA-4 antibody for metastatic melanoma. Clin Cancer Res 2011, 17:6958-6962.