EBV infection determines the immune hallmarks of plasmablastic lymphoma

References

• Delecluse HJ, Anagnostopoulos I, Dallenbach F, Hummel M, Marafioti T, Schneider U, Huhn D, Schmidt-Westhausen A, Reichart PA, Gross U, et al. Plasmablastic lymphomas of the oral cavity: a new entity associated with the human immunodeficiency virus infection. Blood. 1997;89:1413–1420.
   PubMed Web of Science ®Google Scholar
• Castillo JJ, Reagan JL. Plasmablastic lymphoma: a systematic review. ScientificWorldJournal. 2011;11:687–696. doi:10.1100/tsw.2011.59.
   PubMedGoogle Scholar
• Rafaniello Raviele P, Pruneri G, Maiorano E. Plasmablastic lymphoma: a review. Oral Dis. 2009;15:38–45. doi:10.1111/j.1601-0825.2008.01493.x.
   PubMed Web of Science ®Google Scholar
• Colomo L, Loong F, Rives S, Pittaluga S, Martinez A, Lopez-Guillermo A, Ojanguren J, Romagosa V, Jaffe ES, Campo E. Diffuse large B-cell lymphomas with plasmablastic differentiation represent a heterogeneous group of disease entities. Am J Surg Pathol. 2004;28:736–747. doi:10.1097/01.pas.0000126781.87158.e3.
   PubMed Web of Science ®Google Scholar
• Morscio J, Dierickx D, Nijs J, Verhoef G, Bittoun E, Vanoeteren X, Wlodarska I, Sagaert X, Tousseyn T. Clinicopathologic comparison of plasmablastic lymphoma in HIV-positive, immunocompetent, and posttransplant patients: single-center series of 25 cases and meta-analysis of 277 reported cases. Am J Surg Pathol. 2014;38:875–886. doi:10.1097/PAS.0000000000000234.
   PubMed Web of Science ®Google Scholar
• Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, Thiele J, Vardiman JW. WHO classification of tumours of haematopoietic and lymphoid tissues, 4th Edition. In: IARC Presse L, Lyon. 2008. p. 439.
   Google Scholar
• Lee OJ, Kim KW, Lee GK. Epstein-Barr virus and human immunodeficiency virus-negative oral plasmablastic lymphoma. J Oral Pathol Med. 2006;35:382–384. doi:10.1111/j.1600-0714.2006.00422.x.
   PubMed Web of Science ®Google Scholar
• Loghavi S, Alayed K, Aladily TN, Zuo Z, Ng SB, Tang G, Hu S, Yin CC, Miranda RN, Medeiros LJ, et al. Stage, age, and EBV status impact outcomes of plasmablastic lymphoma patients: a clinicopathologic analysis of 61 patients. J Hematol Oncol. 2015;8:65. doi:10.1186/s13045-015-0163-z.
   PubMed Web of Science ®Google Scholar
• Laurent C, Fabiani B, Do C, Tchernonog E, Cartron G, Gravelle P, Amara N, Malot S, Palisoc MM, Copie-Bergman C, et al. Immune-checkpoint expression in Epstein-Barr virus positive and negative plasmablastic lymphoma: a clinical and pathological study in 82 patients. Haematologica. 2016;101:976–984. doi:10.3324/haematol.2016.141978.
   PubMed Web of Science ®Google Scholar
• Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer. 2012;12:252–264. doi:10.1038/nrc3239.
   PubMed Web of Science ®Google Scholar
• Andorsky DJ, Yamada RE, Said J, Pinkus GS, Betting DJ, Timmerman JM. Programmed death ligand 1 is expressed by non-hodgkin lymphomas and inhibits the activity of tumor-associated T cells. Clin Cancer Res. 2011;17:4232–4244. doi:10.1158/1078-0432.CCR-10-2660.
   PubMed Web of Science ®Google Scholar
• Armand P. Checkpoint blockade in lymphoma. Hematology/The Educ Program Am Soc Hematol Am Soc Hematol Educ Program. 2015;2015:69–73.
   PubMedGoogle Scholar
• Laurent C, Charmpi K, Gravelle P, Tosolini M, Franchet C, Ysebaert L, Brousset P, Bidaut A, Ycart B, Fournié JJ. Several immune escape patterns in non-Hodgkin’s lymphomas. Oncoimmunology. 2015;4:e1026530. doi:10.1080/2162402X.2015.1026530.
   PubMed Web of Science ®Google Scholar
• Ninomiya S, Hara T, Tsurumi H, Hoshi M, Kanemura N, Goto N, Kasahara S, Shimizu M, Ito H, Saito K, et al. Indoleamine 2,3-dioxygenase in tumor tissue indicates prognosis in patients with diffuse large B-cell lymphoma treated with R-CHOP. Ann Hematol. 2011;90:409–416. doi:10.1007/s00277-010-1093-z.
   PubMed Web of Science ®Google Scholar
• Löb S, Königsrainer A, Rammensee HG, Opelz G, Terness P. Inhibitors of indoleamine-2,3-dioxygenase for cancer therapy: can we see the wood for the trees? Nat Rev Cancer. 2009;9:445–452. doi:10.1038/nrc2639.
   PubMed Web of Science ®Google Scholar
• Munn DH, Mellor AL. Indoleamine 2,3-dioxygenase and tumor-induced tolerance. J Clin Invest. 2007;117:1147–1154. doi:10.1172/JCI31178.
   PubMed Web of Science ®Google Scholar
• Rodríguez PC, Ochoa AC. Arginine regulation by myeloid derived suppressor cells and tolerance in cancer: mechanisms and therapeutic perspectives. Immunol Rev. 2008;222:180–191. doi:10.1111/j.1600-065X.2008.00608.x.
   PubMed Web of Science ®Google Scholar
• Sun Z, Fourcade J, Pagliano O, Chauvin JM, Sander C, Kirkwood JM, Zarour HM. IL10 and PD-1 cooperate to limit the activity of tumor-specific CD8+ T cells. Cancer Res. 2015;75(8):1635–1644. doi:10.1158/0008-5472.CAN-14-3016.
   Web of Science ®Google Scholar
• Roberts AB, Thompson NL, Heine U, Flanders C, Sporn MB. Transforming growth factor-beta: possible roles in carcinogenesis. Br J Cancer. 1988;57:594–600. doi:10.1038/bjc.1988.135.
   PubMed Web of Science ®Google Scholar
• Sharma S, Stolina M, Lin Y, Gardner B, Miller PW, Kronenberg M, Dubinett SM. T cell-derived IL-10 promotes lung cancer growth by suppressing both T cell and APC function. J Immunol. 1999;163:5020–5028.
   PubMed Web of Science ®Google Scholar
• Curiel TJ, Coukos G, Zou L, Alvarez X, Cheng P, Mottram P, Evdemon-Hogan M, Conejo-Garcia JR, Zhang L, Burow M, et al. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med. 2004;10:942–949. doi:10.1038/nm1093.
   PubMed Web of Science ®Google Scholar
• Yang ZZ, Novak AJ, Ziesmer SC, Witzig TE, Ansell SM. Attenuation of CD8(+) T-cell function by CD4(+)CD25(+) regulatory T cells in B-cell non-Hodgkin’s lymphoma. Cancer Res. 2006;66:10145–10152. doi:10.1158/0008-5472.CAN-06-1822.
   PubMed Web of Science ®Google Scholar
• Alvaro T, Lejeune M, Camacho FI, Salvadó MT, Sánchez L, García JF, Lopez C, Jaén J, Bosch R, Pons LE, et al. The presence of STAT1-positive tumor-associated macrophages and their relation to outcome in patients with follicular lymphoma. Haematologica. 2006;91:1605–1612.
   PubMed Web of Science ®Google Scholar
• al-Sarireh B, Eremin O. Tumour-associated macrophages (TAMS): disordered function, immune suppression and progressive tumour growth. J R Coll Surg Edinb. 2000;45:1–16.
   PubMedGoogle Scholar
• Azzaoui I, Uhel F, Rossille D, Pangault C, Dulong J, Le Priol J, Lamy T, Houot R, Le Gouill S, Cartron G, et al. T-cell defect in diffuse large B-cell lymphomas involves expansion of myeloid-derived suppressor cells. Blood. 2016;128:1081–1092. doi:10.1182/blood-2015-08-662783.
   PubMed Web of Science ®Google Scholar
• Tosolini M, Algans C, Pont F, Ycart B, Fournié -J-J. Large scale microarray profiling reveals four stages of immune escape in non-Hodgkin lymphomas. Oncoimmunology. 2016;5. doi:10.1080/2162402X.2016.1188246.
   PubMed Web of Science ®Google Scholar
• Gu L, Tseng S, Horner RM, Tam C, Loda M, Rollins BJ. Control of TH2 polarization by the chemokine monocyte chemoattractant protein-1. Nature. 2000;404:407–411. doi:10.1038/35006097.
   PubMed Web of Science ®Google Scholar
• Yang ZZ, Grote DM, Ziesmer SC, Niki T, Hirashima M, Novak AJ, Witzig TE, Ansell SM. IL-12 upregulates TIM-3 expression and induces T cell exhaustion in patients with follicular B cell non-Hodgkin lymphoma. J Clin Invest. 2012;122:1271–1282. doi:10.1172/JCI59806.
   PubMed Web of Science ®Google Scholar
• Kridel R, Xerri L, Gelas-Dore B, Tan K, Feugier P, Vawda A, Canioni D, Farinha P, Boussetta S, Moccia AA, et al. The prognostic impact of CD163-positive macrophages in follicular lymphoma: a study from the bc cancer agency and the lymphoma study association. Clin Cancer Res. 2015;21:3428–3435. doi:10.1158/1078-0432.CCR-14-3253.
   PubMed Web of Science ®Google Scholar
• Yang ZZ, Grote DM, Ziesmer SC, Xiu B, Novak AJ, Ansell SM. PD-1 expression defines two distinct T-cell sub-populations in follicular lymphoma that differentially impact patient survival. Blood Cancer J. 2015;5:e281. doi:10.1038/bcj.2015.1.
   PubMed Web of Science ®Google Scholar
• Muenst S, Hoeller S, Willi N, Dirnhofera S, Tzankov A. Diagnostic and prognostic utility of PD-1 in B cell lymphomas. Dis Markers. 2010;29:47–53. doi:10.1155/2010/404069.
   PubMed Web of Science ®Google Scholar
• Gravelle P, Do C, Franchet C, Mueller S, Oberic L, Ysebaert L, Larocca LM, Hohaus S, Calmels MN, Frenois FX, et al. Impaired functional responses in follicular lymphoma CD8(+)TIM-3(+) T lymphocytes following TCR engagement. Oncoimmunology. 2016;5:e1224044. doi:10.1080/2162402X.2016.1224044.
   PubMed Web of Science ®Google Scholar
• Dodd LE, Sengupta S, Chen IH, Den Boon JA, Cheng YJ, Westra W, Newton MA, Mittl BF, McShane L, Chen CJ, et al. Genes involved in DNA repair and nitrosamine metabolism and those located on chromosome 14q32 are dysregulated in nasopharyngeal carcinoma. Cancer Epidemiol Biomarkers Prev. 2006;15:2216–2225. doi:10.1158/1055-9965.EPI-06-0455.
   PubMed Web of Science ®Google Scholar
• Cristescu R, Lee J, Nebozhyn M, Km K, Ting JC, Wong SS, Liu J, Yue YG, Wang J, Yu K, et al. Molecular analysis of gastric cancer identifies subtypes associated with distinct clinical outcomes. Nat Med. 2015;21:449–456. doi:10.1038/nm.3850.
   PubMed Web of Science ®Google Scholar
• Newman AM, Liu CL, Green MR, Gentles AJ, Feng W, Xu Y, Hoang CD, Diehn M, Alizadeh AA. Robust enumeration of cell subsets from tissue expression profiles. Nat Methods. 2015;12:453–457. doi:10.1038/nmeth.3337.
   PubMed Web of Science ®Google Scholar
• Rooney MS, Shukla SA, Wu CJ, Getz G, Hacohen N. Molecular and genetic properties of tumors associated with local immune cytolytic activity. Cell. 2015;160:48–61. doi:10.1016/j.cell.2014.12.033.
   PubMed Web of Science ®Google Scholar
• Giulino-Roth L, Wang K, MacDonald TY, Mathew S, Tam Y, Cronin MT, Palmer G, Lucena-Silva N, Pedrosa F, Pedrosa M, et al. Targeted genomic sequencing of pediatric Burkitt lymphoma identifies recurrent alterations in antiapoptotic and chromatin-remodeling genes. Blood. 2012;120:5181–5184. doi:10.1182/blood-2012-06-437624.
   PubMed Web of Science ®Google Scholar
• Onnis A, Navari M, Antonicelli G, Morettini F, Mannucci S, De Falco G, Vigorito E, Leoncini L. Epstein-Barr nuclear antigen 1 induces expression of the cellular microRNA hsa-miR-127 and impairing B-cell differentiation in EBV-infected memory B cells. New insights into the pathogenesis of Burkitt lymphoma. Blood Cancer J. 2012;2:e84. doi:10.1038/bcj.2012.29.
   PubMed Web of Science ®Google Scholar
• Navari M, Fuligni F, Laginestra MA, Etebari M, Ambrosio MR, Sapienza MR, Rossi M, De Falco G, Gibellini D, Tripodo C, et al. Molecular signature of Epstein Barr virus-positive Burkitt lymphoma and post-transplant lymphoproliferative disorder suggest different roles for Epstein Barr virus. Front Microbiol. 2014;5:728. doi:10.3389/fmicb.2014.00728.
   PubMed Web of Science ®Google Scholar
• Shi M, Gan YJ, Davis TO, Scott RS. Downregulation of the polyamine regulator spermidine/spermine N(1)-acetyltransferase by Epstein-Barr virus in a Burkitt’s lymphoma cell line. Virus Res. 2013;177:11–21. doi:10.1016/j.virusres.2013.07.004.
   PubMed Web of Science ®Google Scholar
• Morscio J, Finalet Ferreiro J, Vander Borght S, Bittoun E, Gheysens O, Dierickx D, Verhoef G, Wlodarska I, Tousseyn T. Identification of distinct subgroups of EBV-positive post-transplant diffuse large B-cell lymphoma. Mod Pathol. 2017;30:370–381. doi:10.1038/modpathol.2016.199.
   PubMed Web of Science ®Google Scholar
• Morscio J, Dierickx D, Ferreiro JF, Herreman A, Van Loo P, Bittoun E, Verhoef G, Matthys P, Cools J, Wlodarska I, et al. Gene expression profiling reveals clear differences between EBV-positive and EBV-negative posttransplant lymphoproliferative disorders. Am J Transplant. 2013;13:1305–1316. doi:10.1111/ajt.12196.
   PubMed Web of Science ®Google Scholar
• Hude I, Sasse S, Engert A, Bröckelmann PJ. The emerging role of immune checkpoint inhibition in malignant lymphoma. Haematologica. 2017;102:30–42. doi:10.3324/haematol.2016.150656.
   PubMed Web of Science ®Google Scholar
• Roemer MGM, Redd RA, Cader FZ, Pak CJ, Abdelrahman S, Ouyang J, Sasse S, Younes A, Fanale M, Santoro A, et al. Major histocompatibility complex class ii and programmed death ligand 1 expression predict outcome after programmed death 1 blockade in classic hodgkin lymphoma. J Clin Oncol. 2018;36:942–950. doi:10.1200/JCO.2017.77.3994.
   PubMed Web of Science ®Google Scholar
• Laurent C, Baron M, Amara N, Haioun C, Dandoit M, Maynadié M, Parrens M, Vergier B, Copie-Bergman C, Fabiani B, et al. Impact of expert pathologic review of lymphoma diagnosis: study of patients from the french lymphopath network. J Clin Oncol. 2017;35:2008–2017. doi:10.1200/JCO.2016.71.2083.
   PubMed Web of Science ®Google Scholar
• Swerdlow SH, Campo E, Pileri SA, Harris NL, Stein H, Siebert R, Advani R, Ghielmini M, Salles GA, Zelenetz AD, et al. The 2016 revision of the World Health Organization classification of lymphoid neoplasms. Blood. 2016;127:2375–2390. doi:10.1182/blood-2016-01-643569.
   PubMed Web of Science ®Google Scholar
• Laurent C, Guérin M, Frenois FX, Thuries V, Jalabert L, Brousset P, Valmary-Degano S. Whole-slide imaging is a robust alternative to traditional fluorescent microscopy for fluorescence in situ hybridization imaging using break-apart DNA probes. Hum Pathol. 2013;44:1544–1555. doi:10.1016/j.humpath.2012.12.009.
   PubMed Web of Science ®Google Scholar
• Steidl C, Shah SP, Woolcock BW, Rui L, Kawahara M, Farinha P, Johnson NA, Zhao Y, Telenius A, Neriah SB, et al. MHC class II transactivator CIITA is a recurrent gene fusion partner in lymphoid cancers. Nature. 2011;471:377–381. doi:10.1038/nature09754.
   PubMed Web of Science ®Google Scholar
• Gentles AJ, Newman AM, Liu CL, Bratman SV, Feng W, Kim D, Nair VS, Xu Y, Khuong A, Hoang CD, et al. The prognostic landscape of genes and infiltrating immune cells across human cancers. Nat Med. 2015;21:938–945. doi:10.1038/nm.3909.
   PubMed Web of Science ®Google Scholar
• Bindea G, Mlecnik B, Hackl H, Charoentong P, Tosolini M, Kirilovsky A, Fridman WH, Pagès F, Trajanoski Z, Galon J. ClueGO: a Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks. Bioinformatics. 2009;25:1091–1093. doi:10.1093/bioinformatics/btp101.
   PubMed Web of Science ®Google Scholar