PD-1 Blockade can restore functions of tcells in Epstein-Barr virus-positive diffuse large b-cell lymphoma in vitro

PLoS ONE

Volumn 10, Issue 9, 2015, Pages

  Quan, Lina ^a   Chen, Xue ^a   Liu, Aichun ^a   Zhang, Yan ^a   Guo, Xiuchen ^a   Yan, Shujie ^a   Liu, Yue ^a  

^a HARBIN MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CD45RO ANTIGEN; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; EPSTEIN BARR VIRUS ANTIGEN; EPSTEIN BARR VIRUS ANTIGEN 2; EPSTEIN BARR VIRUS ANTIGEN 3A; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 2; LACTATE DEHYDROGENASE; PROGRAMMED DEATH 1 RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; CYTOKINE;

ADULT; ARTICLE; CD8+ T LYMPHOCYTE; CELL INFILTRATION; COCULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; EFFECTOR CELL; EPSTEIN BARR VIRUS; EPSTEIN BARR VIRUS INFECTION; FEMALE; FLOW CYTOMETRY; GERMINAL CENTER; HEMATOLOGIC MALIGNANCY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNE SYSTEM; INTERNATIONAL PROGNOSTIC INDEX; LACTATE DEHYDROGENASE BLOOD LEVEL; LARGE CELL LYMPHOMA; LYMPHOMA CELL LINE; MAJOR CLINICAL STUDY; MALE; MEMORY T LYMPHOCYTE; PROTEIN EXPRESSION; T CELL LYMPHOMA; TUMOR IMMUNITY; TUMOR MICROENVIRONMENT; VIRUS LATENCY; AGED; ANTAGONISTS AND INHIBITORS; CANCER STAGING; CASE CONTROL STUDY; COMPLICATION; DIFFUSE LARGE B CELL LYMPHOMA; GENE EXPRESSION; GENETICS; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; MIDDLE AGED; MIXED LYMPHOCYTE CULTURE; PATHOLOGY; PHENOTYPE; T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION; TRANSFORMED CELL LINE; TUMOR CELL LINE; VERY ELDERLY; VIROLOGY;

AGED; AGED, 80 AND OVER; CASE-CONTROL STUDIES; CELL LINE, TRANSFORMED; CELL LINE, TUMOR; CYTOKINES; EPSTEIN-BARR VIRUS INFECTIONS; GENE EXPRESSION; HERPESVIRUS 4, HUMAN; HUMANS; IMMUNOLOGIC MEMORY; LYMPHOCYTE ACTIVATION; LYMPHOCYTE CULTURE TEST, MIXED; LYMPHOMA, LARGE B-CELL, DIFFUSE; MIDDLE AGED; NEOPLASM STAGING; PHENOTYPE; PROGRAMMED CELL DEATH 1 RECEPTOR; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES; TUMOR MICROENVIRONMENT;

EID: 84975775427     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0136476     Document Type: Article

References (49)

1. de Visser KE, Eichten A, Coussens LM. Paradoxical roles of the immune system during cancer development. Nat Rev Cancer 2006; 6:24-37.
2. Shankaran V, Ikeda H, Bruce AT, White JM, Swanson PE, Old LJ, et al. IFNgamma and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature 2001; 410:1107-1111.
3. Bryan LJ, Gordon LI. Blocking tumor escape in hematologic malignancies: The anti-PD-1 strategy. Blood Rev 2015; 29(1):25-32.
4. Ok CY1, Papathomas TG, Medeiros LJ, Young KH. EBV-positive diffuse large B-cell lymphoma of the elderly. Blood 2013; 122: 328-340. doi: 10.1182/blood-2013-03-489708
5. Francisco LM, Sage PT, Sharpe AH. The PD-1 pathway in tolerance and autoimmunity. Immunol Rev 2010; 236:219-242. doi: 10.1111/j.1600-065X.2010.00923.x
6. Kuchroo VK, Anderson AC, Petrovas C. Coinhibitory receptors and CD8 T cell exhaustion in chronic infections. Curr Opin HIV AIDS 2014; 9:439-445.
7. Barber DL, Wherry EJ, Masopust D, Zhu B, Allison JP, Sharpe AH, et al. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 2006; 439:682-687.
8. Jacobsen ED. Restoring antitumor immunity via PD-1 blockade after autologous stem-cell transplantation for diffuse large B-cell lymphoma. J Clin Oncol 2013; 31:4268-4270. doi: 10.1200/JCO.2013.51. 7680
9. Carreras J, Lopez-Guillermo A, Roncador G, Villamor N, Colomo L, Martinez A, et al. High numbers of tumor-infiltrating programmed cell death 1-positive regulatory lymphocytes are associated with improved overall survival in follicular lymphoma. J Clin Oncol 2009; 27:1470-1476. doi: 10.1200/JCO. 2008.18.0513
10. Tzankov A, Meier C, Hirschmann P, Went P, Pileri SA, Dirnhofer S. Correlation of high numbers of intratumoral FOXP3+ regulatory T cells with improved survival in germinal center-like diffuse large B-cell lymphoma, follicular lymphoma and classical Hodgkin's lymphoma. Haematologica 2008; 93:193-200. doi: 10.3324/haematol.11702
11. Muenst S, Hoeller S, Dirnhofer S, Tzankov A. Increased programmed death-1+ tumor-infiltrating lymphocytes in classical Hodgkin lymphoma substantiate reduced overall survival. Hum Pathol 2009; 40:1715-1722. doi: 10.1016/j.humpath.2009.03.025
12. Chen L. Co-inhibitory molecules of the B7-CD28 family in the control of T-cell immunity. Nat Rev Immunol 2004; 4:336-347.
13. Armand P, Nagler A, Weller EA, Devine SM, Avigan DE, Chen YB, et al. Disabling immune tolerance by programmed death-1 blockade with pidilizumab after autologous hematopoietic stem-cell transplantation for diffuse large B-cell lymphoma: results of an international phase II trial. J Clin Oncol 2013; 31:4199-4206. doi: 10.1200/JCO.2012.48.3685
14. Westin JR, Chu F, Zhang M, Fayad LE, Kwak LW, Fowler N, et al. Safety and activity of PD1 blockade by pidilizumab in combination with rituximab in patients with relapsed follicular lymphoma: A single group, open-label, phase 2 trial. Lancet Oncol 2014; 15:69-77. doi: 10.1016/S1470-2045(13)70551-5
15. Dong H, Strome SE, Salomao DR, Tamura H, Hirano F, Flies DB, et al. Tumor-Associated B7-H1 promotes T-cell apoptosis:A potential mechanism of immune evasion. Nat Med 2002; 8:793-800.
16. 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
17. Chen BJ, Chapuy B, Ouyang J, Sun HH, Roemer MG, Xu ML, et al. PD-L1 Expression Is Characteristic of a Subset of Aggressive B-cell Lymphomas and Virus-Associated Malignancies. Clin Cancer Res 2013; 19:3462-3473. doi: 10.1158/1078-0432.CCR-13-0855
18. Hui-Yuen J, McAllister S, Koganti S, Hill E, Bhaduri-McIntosh S. Establishment of Epstein-Barr virus growth-Transformed lymphoblastoid cell lines. J Vis Exp 2011; 8.
19. IARC. WHO classification of tumours of haematopoietic and lymphoid tissues, 4th edn., vol. 2. Lyon: WHO Press, 2008.
20. Hans CP, Weisenburger DD, Greiner TC, Gascoyne RD, Delabie J, Ott G, et al. Confirmation of the molecular classification of diffuse large B-cell lymphoma by immunohistochemistry using a tissue microarray. Blood 2004; 103:275-282.
21. Lu CH, Lee KF, Chen CC, Chen YY, Huang CE, Tsai PS, et al. Clinical characteristics and treatment outcome in a Taiwanese population of patients with Epstein-Barr virus-positive diffuse large B-cell lympho-ma. Jpn J Clin Oncol 2014; 44:1164-1171. doi: 10.1093/jjco/hyu155
22. Oyama T, Yamamoto K, Asano N, Oshiro A, Suzuki R, Kagami Y, et al. Age-related EBV-Associated BCell lymphoproliferative disorders constitute a distinct clinicopathologic group: A study of 96 patients. Clin Cancer Res 2007; 13:5124-5132.
23. Quah BJ, Parish CR. The use of carboxyfluorescein diacetate succinimidyl ester (CFSE) to monitor lymphocyte proliferation. J Vis Exp 2010;12-44.
24. Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer 2012; 12:252-264. doi: 10.1038/nrc3239
25. Blackburn SD, Shin H, Haining WN, Zou T, Workman CJ, Polley A, et al. Coregulation of CD8+ T cell exhaustion by multiple inhibitory receptors during chronic viral infection. Nat Immunol 2009; 10:29-37. doi: 10.1038/ni.1679
26. Baitsch L, Baumgaertner P, Devêvre E, Raghav SK, Legat A, Barba L, et al. Exhaustion of tumorspecific CD8(+) T cells in metastases from melanoma patients. J Clin Invest 2011; 121:2350-2360. doi: 10.1172/JCI46102
27. Yang ZZ, Novak AJ, Stenson MJ, Witzig TE, Ansell SM. Intratumoral CD4+CD25+ Regulatory T-cellmediated suppression of infiltrating CD4+ T cells in B-cell non-Hodgkin lymphoma. Blood 2006; 107:3639-3946.
28. Chen DS, Irving BA, Hodi FS. Molecular pathways: next-generation immunotherapy-inhibiting programmed death-ligand 1 and programmed death-1. Clin Cancer Res 2012; 18(24):6580-6587 doi: 10. 1158/1078-0432.CCR-12-1362
29. Gao Q, Wang XY, Qiu SJ, Yamato I, Sho M, Nakajima Y, et al. Overexpression of PD-L1 significantly associates with tumor aggressiveness and postoperative recurrence in human hepatocellular carcinoma. Clin Cancer Res 2009; 15(3):971-979 doi: 10.1158/1078-0432.CCR-08-1608
30. Hino R, Kabashima K, Kato Y, Yagi H, Nakamura M, Honjo T, et al. Tumor cell expression of programmed cell death-1 ligand 1 is a prognostic factor for malignant melanoma. Cancer 2010; 116 (7):1757-1766 doi: 10.1002/cncr.24899
31. Mu CY, Huang JA, Chen Y, Chen C, Zhang XG. High expression of PD-L1 in lung cancer may contribute to poor prognosis and tumor cells immune escape through suppressing tumor infiltrating dendritic cells maturation. Med Oncol 2011; 28(3):682-688 doi: 10.1007/s12032-010-9515-2
32. Green MR, Rodig S, Juszczynski P, Ouyang J, Sinha P, O'Donnell E, et al. Constitutive AP-1 activity and EBV infection induce PD-L1 in Hodgkin lymphomas and posttransplant lymphoproliferative disorders: implications for targeted therapy. Clin Cancer Res 2012; 18(6):1611-1618. doi: 10.1158/1078-0432.CCR-11-1942
33. Wang BJ, Bao JJ, Wang JZ, Wang Y, Jiang M, Xing MY, et al. Immunostaining of PD-1/PD-Ls in liver tissues of patients with hepatitis and hepatocellular carcinoma. World J Gastroenterol 2011; 17 (28):3322-3329. doi: 10.3748/wjg.v17.i28.3322
34. Lyford-Pike S, Peng S, Young GD, Taube JM, Westra WH, Akpeng B, et al. Evidence for a role of the PD-1:PD-L1 pathway in immune resistance of HPV-Associated head and neck squamous cell carcinoma. Cancer Res 2013; 73(6):1733-1741. doi: 10.1158/0008-5472.CAN-12-2384
35. Badoual C, Hans S, Merillon N, Van Ryswick C, Ravel P, Benhamouda N, et al. PD-1-expressing tumor-infiltrating T cells are a favorable prognostic biomarker in HPV-Associated head and neck cancer. Cancer Res 2013; 73(1):128-138. doi: 10.1158/0008-5472.CAN-12-2606
36. Fang W, Zhang J, Hong S, Zhan J, Chen N, Qin T, et al. EBV-driven LMP1 and IFN-γ up-regulate PDL1 in nasopharyngeal carcinoma: Implications for oncotargeted therapy. Oncotarget 2014; 5 (23):12189-12202.
37. Green MR, Monti S, Rodig SJ, Juszczynski P, Currie T, O'Donnell E, et al. Integrative analysis reveals selective 9p24.1 amplification, increased PD-1 ligand expression, and further induction via JAK2 in nodular sclerosing Hodgkin lymphoma and primary mediastinal large B-cell lymphoma. Blood 2010; 116:3268-3277. doi: 10.1182/blood-2010-05-282780
38. Marzec M, Zhang Q, Goradia A, Raghunath PN, Liu X, Paessler M, et al. Oncogenic kinase NPM/ALK induces through STAT3 expression of immunosuppressive protein CD274 (PD-L1, B7-H1). Proc Natl Acad Sci U S A 2008; 105(52):20852-20857. doi: 10.1073/pnas.0810958105
39. Dong H, Zhu G, Tamada K, Chen L. B7-H1, a third member of the B7 family, co-stimulates T-cell proliferation and interleukin-10 secretion. Nat Med 1999; 5:1365-1369.
40. Shinohara T, Taniwaki M, Ishida Y, Kawaichi M, Honjo T. Structure and chromosomal localization of the human PD-1 gene (PDCD1). Genomics 1994; 23:704-706.
41. Hamilton-Dutoit SJ, Rea D, Raphael M, Sandvej K, Delecluse HJ, Gisselbrecht C, et al. Epstein-Barr virus-latent gene expression and tumor cell phenotype in acquired immunodeficiency syndrome-related non-Hodgkin's lymphoma. Correlation of lymphoma phenotype with three distinct patterns of viral latency. Am J Pathol 1993; 143:1072-1085.
42. Wherry EJ.T cell exhaustion.Nat Immunol 2011; 12:492-499.
43. Ansell SM, Hurvitz SA, Koenig PA, LaPlant BR, Kabat BF, Fernando D, et al. Phase I study of ipilimumab, an anti-CTLA-4 monoclonal antibody, in patients with relapsed and refractory B-cell non-Hodgkin lymphoma. Clin Cancer Res 2009; 15:6446-6453. doi: 10.1158/1078-0432.CCR-09-1339
44. Wolchok JD, Kluger H, Callahan MK, Postow MA, Rizvi NA, Lesokhin AM, et al. Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med 2013; 369:122-133. doi: 10.1056/NEJMoa1302369
45. Schuster SJ, Neelapu SS, Gause BL, Janik JE, Muggia FM, Gockerman JP, et al. Vaccination with patient specific tumor-derived antigen in first remission improves disease-free survival in follicular lymphoma. J Clin Oncol 2011; 29:2787-2794. doi: 10.1200/JCO.2010.33.3005
46. Houot R, Levy R. T-cell modulation combined with intratumoral CpG cures lymphoma in a mouse model without the need for chemotherapy. Blood 2009; 113: 3546-3552. doi: 10.1182/blood-2008-07-170274
47. Houot R, Goldstein MJ, Kohrt HE, Myklebust JH, Alizadeh AA, Lin JT, et al. Therapeutic effect of CD137 immunomodulation in lymphoma and its enhancement by Treg depletion. Blood 2009; 114:3431-3438. doi: 10.1182/blood-2009-05-223958
48. Curran MA, Montalvo W, Yagita H, Allison JP. PD-1 and CTLA-4 combination blockade expands infiltrating T cells and reduces regulatory T and myeloid cells within B16 melanoma tumors. Proc Natl Acad Sci U S A 2010; 107(9):4275-4280. doi: 10.1073/pnas.0915174107
49. Zhou Q, Xiao H, Liu Y, Peng Y, Hong Y, Yagita H, et al. Blockade of programmed death-1 pathway rescues the effector function of tumor-infiltrating T cells and enhances the antitumor efficacy of lentivector immunization. J Immunol 2010; 185(9):5082-5092. doi: 10.4049/jimmunol.1001821