Lymphoma immunotherapy: Current status

Frontiers in Immunology

Volumn 6, Issue SEP, 2015, Pages 448-

  Zappasodi, Roberta ^a   de Braud, Filippo ^b   Di Nicola, Massimo ^b  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b NATIONAL CANCER INSTITUTE   (Italy)

Author keywords

Adaptive immune response; Anticancer vaccines; B cell lymphoma; Dendritic cells; Immunotherapy; Tumor associated antigens

Indexed keywords

CD20 ANTIGEN; CHIMERIC ANTIGEN RECEPTOR; CYCLOPHOSPHAMIDE; DOXORUBICIN; KEYHOLE LIMPET HEMOCYANIN; PREDNISONE; RITUXIMAB; TOLL LIKE RECEPTOR; TUMOR ANTIGEN; VACCINE; VINCRISTINE;

CANCER IMMUNOTHERAPY; CANCER SURVIVAL; CELL THERAPY; CLINICAL ASSESSMENT; CLINICAL TRIAL (TOPIC); CYTOTOXIC T LYMPHOCYTE; DRUG SAFETY; GLYCOSYLATION; HUMAN; IMMUNOGENICITY; IMMUNOMODULATION; IMMUNOSUPPRESSIVE TREATMENT; LARGE CELL LYMPHOMA; LYMPHOMA; NATURAL KILLER CELL; NONHUMAN; OUTCOME ASSESSMENT; PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); REVIEW; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT; VACCINATION;

EID: 84949654926     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2015.00448     Document Type: Review

References (143)

1. Chao MP. Treatment challenges in the management of relapsed or refractory non-Hodgkin's lymphoma - novel and emerging therapies. Cancer Manag Res (2013) 5:251-69. doi:10.2147/CMAR.S34273
2. Multani P, White CA, Grillo-Lopez A. Non-Hodgkin's lymphoma: review of conventional treatments. Curr Pharm Biotechnol (2001) 2:279-91. doi:10.2174/1389201013378581
3. Leget GA, Czuczman MS. Use of rituximab, the new FDA-approved antibody. Curr Opin Oncol (1998) 10:548-51. doi:10.1097/00001622-199811000-00012
4. Cheson BD, Leonard JP. Monoclonal antibody therapy for B-cell non-Hodgkin's lymphoma. N Engl J Med (2008) 359:613-26. doi:10.1056/NEJMra0708875
5. McLaughlin P, Grillo-Lopez AJ, Link BK, Levy R, Czuczman MS, Williams ME, et al. Rituximab chimeric anti-CD20 monoclonal antibody therapy for relapsed indolent lymphoma: half of patients respond to a four-dose treatment program. J Clin Oncol (1998) 16:2825-33.
6. Davis TA, Grillo-Lopez AJ, White CA, Mclaughlin P, Czuczman MS, Link BK, et al. Rituximab anti-CD20 monoclonal antibody therapy in non-Hodgkin's lymphoma: safety and efficacy of re-treatment. J Clin Oncol (2000) 18:3135-43.
7. Tarella C, Passera R, Magni M, Benedetti F, Rossi A, Gueli A, et al. Risk factors for the development of secondary malignancy after high-dose chemotherapy and autograft, with or without rituximab: a 20-year retrospective follow-up study in patients with lymphoma. J Clin Oncol (2011) 29:814-24. doi:10.1200/JCO.2010.28.9777
8. Rajewsky K. Clonal selection and learning in the antibody system. Nature (1996) 381:751-8. doi:10.1038/381751a0
9. LeBien TW, Tedder TF. B lymphocytes: how they develop and function. Blood (2008) 112:1570-80. doi:10.1182/blood-2008-02-078071
10. Willis TG, Dyer MJ. The role of immunoglobulin translocations in the pathogenesis of B-cell malignancies. Blood (2000) 96:808-22.
11. Küppers R, Dalla-Favera R. Mechanisms of chromosomal translocations in B cell lymphomas. Oncogene (2001) 20:5580-94. doi:10.1038/sj.onc.1204640
12. De Paoli P, Carbone A. Microenvironmental abnormalities induced by viral cooperation: impact on lymphomagenesis. Semin Cancer Biol (2015). doi:10.1016/j.semcancer.2015.03.009
13. Thorley-Lawson DA, Gross A. Persistence of the Epstein-Barr virus and the origins of associated lymphomas. N Engl J Med (2004) 350:1328-37. doi:10.1056/NEJMra032015
14. Young LS, Rickinson AB. Epstein-Barr virus: 40 years on. Nat Rev Cancer (2004) 4:757-68. doi:10.1038/nrc1452
15. Byrd JC, Furman RR, Coutre SE, Flinn IW, Burger JA, Blum KA, et al. Targeting BTK with ibrutinib in relapsed chronic lymphocytic leukemia. N Engl J Med (2013) 369:32-42. doi:10.1056/NEJMoa1215637
16. Wang ML, Rule S, Martin P, Goy A, Auer R, Kahl BS, et al. Targeting BTK with ibrutinib in relapsed or refractory mantle-cell lymphoma. N Engl J Med (2013) 369:507-16. doi:10.1056/NEJMoa1306220
17. Treon SP, Tripsas CK, Meid K, Warren D, Varma G, Green R, et al. Ibrutinib in previously treated Waldenstrom's macroglobulinemia. N Engl J Med (2015) 372:1430-40. doi:10.1056/NEJMoa1501548
18. Gopal AK, Kahl BS, De Vos S, Wagner-Johnston ND, Schuster SJ, Jurczak WJ, et al. PI3Kdelta inhibition by idelalisib in patients with relapsed indolent lymphoma. N Engl J Med (2014) 370:1008-18. doi:10.1056/NEJMoa1314583
19. Eisen HN, Sakato N, Hall SJ. Myeloma proteins as tumor-specific antigens. Transplant Proc (1975) 7:209-14.
20. Janeway CA Jr, Sakato N, Eisen HN. Recognition of immunoglobulin idiotypes by thymus-derived lymphocytes. Proc Natl Acad Sci U S A (1975) 72:2357-60. doi:10.1073/pnas.72.6.2357
21. Herreros B, Sanchez-Aguilera A, Piris MA. Lymphoma microenvironment: culprit or innocent? Leukemia (2008) 22:49-58. doi:10.1038/sj.leu.2404970
22. De Jong D. Molecular pathogenesis of follicular lymphoma: a cross talk of genetic and immunologic factors. J Clin Oncol (2005) 23:6358-63. doi:10.1200/JCO.2005.26.856
23. Dave SS. Follicular lymphoma and the microenvironment. Blood (2008) 111:4427-8. doi:10.1182/blood-2008-01-134643
24. Eray M, Postila V, Eeva J, Ripatti A, Karjalainen-Lindsberg ML, Knuutila S, et al. Follicular lymphoma cell lines, an in vitro model for antigenic selection and cytokine-mediated growth regulation of germinal centre B cells. Scand J Immunol (2003) 57:545-55. doi:10.1046/j.1365-3083.2003.01264.x
25. Goval JJ, Thielen C, Bourguignon C, Greimers R, Dejardin E, Choi YS, et al. The prevention of spontaneous apoptosis of follicular lymphoma B cells by a follicular dendritic cell line: involvement of caspase-3, caspase-8 and c-FLIP. Haematologica (2008) 93:1169-77. doi:10.3324/haematol.12127
26. Yang ZZ, Novak AJ, Stenson MJ, Witzig TE, Ansell SM. Intratumoral CD4+CD25+ regulatory T-cell-mediated suppression of infiltrating CD4+ T cells in B-cell non-Hodgkin lymphoma. Blood (2006) 107:3639-46. doi:10.1182/blood-2005-08-3376
27. Yang ZZ, Novak AJ, Ziesmer SC, Witzig TE, Ansell SM. CD70+ non-Hodgkin lymphoma B cells induce Foxp3 expression and regulatory function in intratumoral CD4+CD25-T cells. Blood (2007) 110:2537-44. doi:10.1182/blood-2007-03-082578
28. Ai WZ, Hou JZ, Zeiser R, Czerwinski D, Negrin RS, Levy R. Follicular lymphoma B cells induce the conversion of conventional CD4+ T cells to T-regulatory cells. Int J Cancer (2009) 124:239-44. doi:10.1002/ijc.23881
29. Farinha P, Masoudi H, Skinnider BF, Shumansky K, Spinelli JJ, Gill K, et al. Analysis of multiple biomarkers shows that lymphoma-associated macrophage (LAM) content is an independent predictor of survival in follicular lymphoma (FL). Blood (2005) 106:2169-74. doi:10.1182/blood-2005-04-1565
30. Alvaro T, Lejeune M, Camacho FI, Salvadó MT, Sánchez L, García JF, et al. The presence of STAT1-positive tumor-associated macrophages and their relation to outcome in patients with follicular lymphoma. Haematologica (2006) 91:1605-12.
31. Tiemessen MM, Jagger AL, Evans HG, Van Herwijnen MJC, John S, Taams LS. CD4+CD25+Foxp3+ regulatory T cells induce alternative activation of human monocytes/macrophages. Proc Natl Acad Sci U S A (2007) 104:19446-51. doi:10.1073/pnas.0706832104
32. Grube M, Rezvani K, Wiestner A, Fujiwara H, Sconocchia G, Melenhorst JJ, et al. Autoreactive, cytotoxic T lymphocytes specific for peptides derived from normal B-cell differentiation antigens in healthy individuals and patients with B-cell malignancies. Clin Cancer Res (2004) 10:1047-56. doi:10.1158/1078-0432.CCR-03-0075
33. Fisher RI, Leblanc M, Press OW, Maloney DG, Unger JM, Miller TP. New treatment options have changed the survival of patients with follicular lymphoma. J Clin Oncol (2005) 23:8447-52. doi:10.1200/JCO.2005.03.1674
34. Friedberg JW. Treatment of follicular non-Hodgkin's lymphoma: the old and the new. Semin Hematol (2008) 45:S2-6. doi:10.1053/j.seminhematol.2008.07.003
35. Hainsworth JD, Litchy S, Shaffer DW, Lackey VL, Grimaldi M, Greco FA. Maximizing therapeutic benefit of rituximab: maintenance therapy versus re-treatment at progression in patients with indolent non-Hodgkin's lymphoma - a randomized phase II trial of the Minnie Pearl Cancer Research Network. J Clin Oncol (2005) 23:1088-95. doi:10.1200/JCO.2005.05.004
36. Park HJ, Neelapu SS. Developing idiotype vaccines for lymphoma: from preclinical studies to phase III clinical trials. Br J Haematol (2008) 142:179-91. doi:10.1111/j.1365-2141.2008.07143.x
37. Khouri IF, Mclaughlin P, Saliba RM, Hosing C, Korbling M, Lee MS, et al. Eight-year experience with allogeneic stem cell transplantation for relapsed follicular lymphoma after nonmyeloablative conditioning with fludarabine, cyclophosphamide, and rituximab. Blood (2008) 111:5530-6. doi:10.1182/blood-2008-01-136242
38. Rezvani AR, Storer B, Maris M, Sorror ML, Agura E, Maziarz RT, et al. Nonmyeloablative allogeneic hematopoietic cell transplantation in relapsed, refractory, and transformed indolent non-Hodgkin's lymphoma. J Clin Oncol (2008) 26:211-7. doi:10.1200/JCO.2007.11.5477
39. Kochenderfer JN, Dudley ME, Kassim SH, Somerville RP, Carpenter RO, Stetler-Stevenson M, et al. Chemotherapy-refractory diffuse large B-cell lymphoma and indolent B-cell malignancies can be effectively treated with autologous T cells expressing an anti-CD19 chimeric antigen receptor. J Clin Oncol (2015) 33:540-9. doi:10.1200/JCO.2014.56.2025
40. Ansell SM, Lesokhin AM, Borrello I, Halwani A, Scott EC, Gutierrez M, et al. PD-1 blockade with nivolumab in relapsed or refractory Hodgkin's lymphoma. N Engl J Med (2015) 372:311-9. doi:10.1056/NEJMoa1411087
41. Postow MA, Chesney J, Pavlick AC, Robert C, Grossmann K, Mcdermott D, et al. Nivolumab and ipilimumab versus ipilimumab in untreated melanoma. N Engl J Med (2015) 372:2006-17. doi:10.1056/NEJMoa1414428
42. Hawkins RE, Russell SJ, Marcus R, Ashworth LJ, Brissnik J, Zhang J, et al. A pilot study of idiotypic vaccination for follicular B-cell lymphoma using a genetic approach. CRC NO: 92/33. Protocol NO: PH1/027. Hum Gene Ther (1997) 8:1287-99.
43. Sakamaki I, Qin H, Kwak LW. Translational development of vaccination strategies in follicular NHL. Best Pract Res Clin Haematol (2011) 24:295-304. doi:10.1016/j.beha.2011.03.007
44. Bendandi M, Gocke CD, Kobrin CB, Benko FA, Sternas LA, Pennington R, et al. Complete molecular remissions induced by patient-specific vaccination plus granulocyte-monocyte colony-stimulating factor against lymphoma. Nat Med (1999) 5:1171-7. doi:10.1038/13928
45. Inoges S, Rodriguez-Calvillo M, Zabalegui N, Lopez-Diaz De Cerio A, Villanueva H, Soria E, et al. Clinical benefit associated with idiotypic vaccination in patients with follicular lymphoma. J Natl Cancer Inst (2006) 98:1292-301. doi:10.1093/jnci/djj358
46. Ai WZ, Tibshirani R, Taidi B, Czerwinski D, Levy R. Anti-idiotype antibody response after vaccination correlates with better overall survival in follicular lymphoma. Blood (2009) 113:5743-6. doi:10.1182/blood-2009-01-201988
47. Neelapu SS, Kwak LW, Kobrin CB, Reynolds CW, Janik JE, Dunleavy K, et al. Vaccine-induced tumor-specific immunity despite severe B-cell depletion in mantle cell lymphoma. Nat Med (2005) 11:986-91. doi:10.1038/nm1290
48. Koc O, Redfern C, Wiernik P, Rosenfelt F, Winter J, Guthrie T, et al. Extended follow-up and analysis with central radiological review of patients receiving FavId® (Id/KLH) vaccine following rituximab. Blood (2005) 106(11):abstr 772.
49. Levy R, Robertson M, Ganjoo K, Leonard J, Vose J, Denney D. Results of a Phase 3 trial evaluating safety and efficacy of specific immunotherapy, recombinant idiotype (Id) conjugated to KLH (Id-KLH) with GM-CSF, compared to non-specific immunotherapy, KLH with GM-CSF, in patients with follicular non-Hodgkin's lymphoma (fNHL). Cancer Res (2008) 68:LB-204.
50. Freedman A, Neelapu SS, Nichols C, Robertson MJ, Djulbegovic B, Winter JN, et al. Placebo-controlled phase III trial of patient-specific immunotherapy with mitumprotimut-T and granulocyte-macrophage colony-stimulating factor after rituximab in patients with follicular lymphoma. J Clin Oncol (2009) 27:3036-43. doi:10.1200/JCO.2008.19.8903
51. 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) 29:2787-94. doi:10.1200/JCO.2010.33.3005
52. Palucka AK, Ueno H, Fay JW, Banchereau J. Taming cancer by inducing immunity via dendritic cells. Immunol Rev (2007) 220:129-50. doi:10.1111/j.1600-065X.2007.00575.x
53. Timmerman JM, Singh G, Hermanson G, Hobart P, Czerwinski DK, Taidi B, et al. Immunogenicity of a plasmid DNA vaccine encoding chimeric idiotype in patients with B-cell lymphoma. Cancer Res (2002) 62:5845-52.
54. King CA, Spellerberg MB, Zhu D, Rice J, Sahota SS, Thompsett AR, et al. DNA vaccines with single-chain Fv fused to fragment C of tetanus toxin induce protective immunity against lymphoma and myeloma. Nat Med (1998) 4:1281-6. doi:10.1038/3266
55. Stevenson FK, Zhu D, King CA, Ashworth LJ, Kumar S, Thompsett A, et al. A genetic approach to idiotypic vaccination for B cell lymphoma. Ann N Y Acad Sci (1995) 772:212-26. doi:10.1111/j.1749-6632.1995.tb44747.x
56. Iurescia S, Fioretti D, Fazio VM, Rinaldi M. Epitope-driven DNA vaccine design employing immunoinformatics against B-cell lymphoma: a biotech's challenge. Biotechnol Adv (2012) 30:372-83. doi:10.1016/j.biotechadv.2011.06.020
57. Brody J, Kohrt H, Marabelle A, Levy R. Active and passive immunotherapy for lymphoma: proving principles and improving results. J Clin Oncol (2011) 29:1864-75. doi:10.1200/JCO.2010.33.4623
58. Rosenberg SA, Yang JC, Restifo NP. Cancer immunotherapy: moving beyond current vaccines. Nat Med (2004) 10:909-15. doi:10.1038/nm1100
59. Timmerman JM. Idiotype-pulsed dendritic cell vaccination for B-cell lymphoma: clinical and immune responses in 35 patients. Blood (2002) 99:1517-26. doi:10.1182/blood.V99.5.1517
60. Franki SN, Steward KK, Betting DJ, Kafi K, Yamada RE, Timmerman JM. Dendritic cells loaded with apoptotic antibody-coated tumor cells provide protective immunity against B-cell lymphoma in vivo. Blood (2008) 111:1504-11. doi:10.1182/blood-2007-03-080507
61. Di Nicola M, Zappasodi R, Carlo-Stella C, Mortarini R, Pupa SM, Magni M, et al. Vaccination with autologous tumor-loaded dendritic cells induces clinical and immunologic responses in indolent B-cell lymphoma patients with relapsed and measurable disease: a pilot study. Blood (2009) 113:18-27. doi:10.1182/blood-2008-06-165654
62. Zappasodi R, Bongarzone I, Ghedini GC, Castagnoli L, Cabras AD, Messina A, et al. Serological identification of HSP105 as a novel non-Hodgkin lymphoma therapeutic target. Blood (2011) 118:4421-30. doi:10.1182/blood-2011-06-364570
63. Zappasodi R, Pupa SM, Ghedini GC, Bongarzone I, Magni M, Cabras AD, et al. Improved clinical outcome in indolent B-cell lymphoma patients vaccinated with autologous tumor cells experiencing immunogenic death. Cancer Res (2010) 70:9062-72. doi:10.1158/0008-5472.CAN-10-1825
64. Zitvogel L, Apetoh L, Ghiringhelli FS, Kroemer G. Immunological aspects of cancer chemotherapy. Nat Rev Immunol (2008) 8:59-73. doi:10.1038/nri2216
65. Wang J, Saffold S, Cao X, Krauss J, Chen W. Eliciting T cell immunity against poorly immunogenic tumors by immunization with dendritic cell-tumor fusion vaccines. J Immunol (1998) 161:5516-24.
66. Van Meirvenne S, Straetman L, Heirman C, Dullaers M, De Greef C, Van Tendeloo V, et al. Efficient genetic modification of murine dendritic cells by electroporation with mRNA. Cancer Gene Ther (2002) 9:787-97. doi:10.1038/sj.cgt.7700499
67. Ni X, Richmond HM, Liao XM, Decker WK, Shiue LH, Shpall EJ, et al. Induction of T-cell responses against cutaneous T-cell lymphomas ex vivo by autologous dendritic cells transfected with amplified tumor mRNA. J Invest Dermatol (2008) 128:2631-9. doi:10.1038/jid.2008.125
68. Winkler C, Steingrube DS, Altermann W, Schlaf G, Max D, Kewitz S, et al. Hodgkin's lymphoma RNA-transfected dendritic cells induce cancer/testis antigen-specific immune responses. Cancer Immunol Immunother (2012) 61:1769-79. doi:10.1007/s00262-012-1239-z
69. Yewdell JW, Norbury CC, Bennink JR. Mechanisms of exogenous antigen presentation by MHC class I molecules in vitro and in vivo: implications for generating CD8+ T cell responses to infectious agents, tumors, transplants, and vaccines. Adv Immunol (1999) 73:1-77. doi:10.1016/S0065-2776(08)60785-3
70. Krieg AM. Development of TLR9 agonists for cancer therapy. J Clin Invest (2007) 117:1184-94. doi:10.1172/JCI31414
71. Brody JD, Ai WZ, Czerwinski DK, Torchia JA, Levy M, Advani RH, et al. In situ vaccination with a TLR9 agonist induces systemic lymphoma regression: a phase I/II study. J Clin Oncol (2010) 28:4324-32. doi:10.1200/JCO.2010.28.9793
72. Kim YH, Gratzinger D, Harrison C, Brody JD, Czerwinski DK, Ai WZ, et al. In situ vaccination against mycosis fungoides by intratumoral injection of a TLR9 agonist combined with radiation: a phase 1/2 study. Blood (2012) 119:355-63. doi:10.1182/blood-2011-05-355222
73. Goldstein MJ, Varghese B, Brody JD, Rajapaksa R, Kohrt H, Czerwinski DK, et al. A CpG-loaded tumor cell vaccine induces antitumor CD4+ T cells that are effective in adoptive therapy for large and established tumors. Blood (2011) 117:118-27. doi:10.1182/blood-2010-06-288456
74. Brody JD, Advani R, Weng W, Czerwinski D, Alizadeh AA, Kohrt HE, et al. Immunotransplant for mantle cell lymphoma: phase I/II study preliminary results. J Clin Oncol (2011) 29(Suppl):abstr 2509.
75. Gottschalk S, Rooney CM, Heslop HE. Post-transplant lymphoproliferative disorders. Annu Rev Med (2005) 56:29-44. doi:10.1146/annurev.med.56.082103.104727
76. Heslop HE. How I treat EBV lymphoproliferation. Blood (2009) 114:4002-8. doi:10.1182/blood-2009-07-143545
77. Thorley-Lawson DA, Gross A. Persistence of the Epstein-Barr virus and the origins of associated lymphomas. N Engl J Med (2004) 350:1328-37. doi:10.1056/NEJMra032015
78. Teslop HE, Slobod KS, Pule MA, Hale GA, Rousseau A, Smith CA, et al. Long-term outcome of EBV-specific T-cell infusions to prevent or treat EBV-related lymphoproliferative disease in transplant recipients. Blood (2010) 115:925-35. doi:10.1182/blood-2009-08-239186
79. Doubrovina E, Oflaz-Sozmen B, Prockop SE, Kernan NA, Abramson S, Teruya-Feldstein J, et al. Adoptive immunotherapy with unselected or EBV-specific T cells for biopsy-proven EBV+ lymphomas after allogeneic hematopoietic cell transplantation. Blood (2012) 119:2644-56. doi:10.1182/blood-2011-08-371971
80. Khanna R, Bell S, Sherritt M, Galbraith A, Burrows SR, Rafter L, et al. Activation and adoptive transfer of Epstein-Barr virus-specific cytotoxic T cells in solid organ transplant patients with posttransplant lymphoproliferative disease. Proc Natl Acad Sci U S A (1999) 96:10391-6. doi:10.1073/pnas.96.18.10391
81. Somoli P, Labirio M, Basso S, Baldanti F, Grossi P, Furione M, et al. Infusion of autologous Epstein-Barr virus (EBV)-specific cytotoxic T cells for prevention of EBV-related lymphoproliferative disorder in solid organ transplant recipients with evidence of active virus replication. Blood (2002) 99:2592-8. doi:10.1182/blood.V99.7.2592
82. Havoldo B, Goss JA, Hammer MM, Zhang L, Lopez T, Gee AP, et al. Treatment of solid organ transplant recipients with autologous Epstein Barr virus-specific cytotoxic T lymphocytes (CTLs). Blood (2006) 108:2942-9. doi:10.1182/blood-2006-05-021782
83. Haque T, Wilkie GM, Jones MM, Higgins CD, Urquhart G, Wingate P, et al. Allogeneic cytotoxic T-cell therapy for EBV-positive posttransplantation lymphoproliferative disease: results of a phase 2 multicenter clinical trial. Blood (2007) 110:1123-31. doi:10.1182/blood-2006-12-063008
84. Barker JN, Doubrovina E, Sauter C, Jaroscak JJ, Perales MA, Doubrovin M, et al. Successful treatment of EBV-associated posttransplantation lymphoma after cord blood transplantation using third-party EBV-specific cytotoxic T lymphocytes. Blood (2010) 116:5045-9. doi:10.1182/blood-2010-04-281873
85. Prockop SE, Doubrovina E, Baroudy K, Boulad F, Khalaf R, Papadopoulos EB, et al. Epstein-Barr virus-specific cytotoxic T lymphocytes for treatment of rituximab-refractory Epstein-Barr virus-associated lymphoproliferative disorder. Cancer Res (2015) 75:CT107. doi:10.1158/1538-7445.AM2015-CT107
86. Bollard CM, Cooper LJ, Heslop HE. Immunotherapy targeting EBV-expressing lymphoproliferative diseases. Best Pract Res Clin Haematol (2008) 21:405-20. doi:10.1016/j.beha.2008.06.002
87. Bollard CM, Gottschalk S, Leen AM, Weiss H, Straathof KC, Carrum G, et al. Complete responses of relapsed lymphoma following genetic modification of tumor-antigen presenting cells and T-lymphocyte transfer. Blood (2007) 110:2838-45. doi:10.1182/blood-2007-05-091280
88. Restifo NP, Dudley ME, Rosenberg SA. Adoptive immunotherapy for cancer: harnessing the T cell response. Nat Rev Immunol (2012) 12:269-81. doi:10.1038/nri3191
89. Eshhar Z, Waks T, Gross G, Schindler DG. Specific activation and targeting of cytotoxic lymphocytes through chimeric single chains consisting of antibody-binding domains and the gamma or zeta subunits of the immunoglobulin and T-cell receptors. Proc Natl Acad Sci U S A (1993) 90:720-4. doi:10.1073/pnas.90.2.720
90. Brentjens RJ, Latouche JB, Santos E, Marti F, Gong MC, Lyddane C, et al. Eradication of systemic B-cell tumors by genetically targeted human T lymphocytes co-stimulated by CD80 and interleukin-15. Nat Med (2003) 9:279-86. doi:10.1038/nm827
91. Cheadle EJ, Hawkins RE, Batha H, Rothwell DG, Ashton G, Gilham DE. Eradication of established B-cell lymphoma by CD19-specific murine T cells is dependent on host lymphopenic environment and can be mediated by CD4+ and CD8+ T cells. J Immunother (2009) 32:207-18. doi:10.1097/CJI.0b013e318194a921
92. James SE, Orgun NN, Tedder TF, Shlomchik MJ, Jensen MC, Lin Y, et al. Antibody-mediated B-cell depletion before adoptive immunotherapy with T cells expressing CD20-specific chimeric T-cell receptors facilitates eradication of leukemia in immunocompetent mice. Blood (2009) 114:5454-63. doi:10.1182/blood-2009-08-232967
93. Kochenderfer JN, Yu Z, Frasheri D, Restifo NP, Rosenberg SA. Adoptive transfer of syngeneic T cells transduced with a chimeric antigen receptor that recognizes murine CD19 can eradicate lymphoma and normal B cells. Blood (2010) 116:3875-86. doi:10.1182/blood-2010-01-265041
94. Cheadle EJ, Hawkins RE, Batha H, O'neill AL, Dovedi SJ, Gilham DE. Natural expression of the CD19 antigen impacts the long-term engraftment but not antitumor activity of CD19-specific engineered T cells. J Immunol (2010) 184:1885-96. doi:10.4049/jimmunol.0901440
95. Kowolik CM, Topp MS, Gonzalez S, Pfeiffer T, Olivares S, Gonzalez N, et al. CD28 costimulation provided through a CD19-specific chimeric antigen receptor enhances in vivo persistence and antitumor efficacy of adoptively transferred T cells. Cancer Res (2006) 66:10995-1004. doi:10.1158/0008-5472.CAN-06-0160
96. Loskog A, Giandomenico V, Rossig C, Pule M, Dotti G, Brenner MK. Addition of the CD28 signaling domain to chimeric T-cell receptors enhances chimeric T-cell resistance to T regulatory cells. Leukemia (2006) 20:1819-28. doi:10.1038/sj.leu.2404366
97. Brentjens RJ, Santos E, Nikhamin Y, Yeh R, Matsushita M, La Perle K, et al. Genetically targeted T cells eradicate systemic acute lymphoblastic leukemia xenografts. Clin Cancer Res (2007) 13:5426-35. doi:10.1158/1078-0432.CCR-07-0674
98. Milone MC, Fish JD, Carpenito C, Carroll RG, Binder GK, Teachey D, et al. Chimeric receptors containing CD137 signal transduction domains mediate enhanced survival of T cells and increased antileukemic efficacy in vivo. Mol Ther (2009) 17:1453-64. doi:10.1038/mt.2009.83
99. Song DG, Ye Q, Carpenito C, Poussin M, Wang LP, Ji C, et al. In vivo persistence, tumor localization, and antitumor activity of CAR-engineered T cells is enhanced by costimulatory signaling through CD137 (4-1BB). Cancer Res (2011) 71:4617-27. doi:10.1158/0008-5472.CAN-11-0422
100. Tammana S, Huang X, Wong M, Milone MC, Ma L, Levine BL, et al. 4-1BB and CD28 signaling plays a synergistic role in redirecting umbilical cord blood T cells against B-cell malignancies. Hum Gene Ther (2010) 21:75-86. doi:10.1089/hum.2009.122
101. Micklethwaite KP, Savoldo B, Hanley PJ, Leen AM, Demmler-Harrison GJ, Cooper LJ, et al. Derivation of human T lymphocytes from cord blood and peripheral blood with antiviral and antileukemic specificity from a single culture as protection against infection and relapse after stem cell transplantation. Blood (2010) 115:2695-703. doi:10.1182/blood-2009-09-242263
102. Terakura S, Yamamoto TN, Gardner RA, Turtle CJ, Jensen MC, Riddell SR. Generation of CD19-chimeric antigen receptor modified CD8+ T cells derived from virus-specific central memory T cells. Blood (2012) 119:72-82. doi:10.1182/blood-2011-07-366419
103. Kochenderfer JN, Wilson WH, Janik JE, Dudley ME, Stetler-Stevenson M, Feldman SA, et al. Eradication of B-lineage cells and regression of lymphoma in a patient treated with autologous T cells genetically engineered to recognize CD19. Blood (2010) 116:4099-102. doi:10.1182/blood-2010-04-281931
104. Porter DL, Levine BL, Kalos M, Bagg A, June CH. Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N Engl J Med (2011) 365:725-33. doi:10.1056/NEJMoa1103849
105. Kochenderfer JN, Dudley ME, Feldman SA, Wilson WH, Spaner DE, Maric I, et al. B-cell depletion and remissions of malignancy along with cytokine-associated toxicity in a clinical trial of anti-CD19 chimeric-antigen-receptor-transduced T cells. Blood (2012) 119:2709-20. doi:10.1182/blood-2011-10-384388
106. Maude SL, Frey N, Shaw PA, Aplenc R, Barrett DM, Bunin NJ, et al. Chimeric antigen receptor T cells for sustained remissions in leukemia. N Engl J Med (2014) 371:1507-17. doi:10.1056/NEJMoa1407222
107. Kochenderfer JN, Dudley ME, Carpenter RO, Kassim SH, Rose JJ, Telford WG, et al. Donor-derived CD19-targeted T cells cause regression of malignancy persisting after allogeneic hematopoietic stem cell transplantation. Blood (2013) 122:4129-39. doi:10.1182/blood-2013-08-519413
108. Cruz CR, Micklethwaite KP, Savoldo B, Ramos CA, Lam S, Ku S, et al. Infusion of donor-derived CD19-redirected virus-specific T cells for B-cell malignancies relapsed after allogeneic stem cell transplant: a phase 1 study. Blood (2013) 122:2965-73. doi:10.1182/blood-2013-06-506741
109. Straathof KC, Pule MA, Yotnda P, Dotti G, Vanin EF, Brenner MK, et al. An inducible caspase 9 safety switch for T-cell therapy. Blood (2005) 105:4247-54. doi:10.1182/blood-2004-11-4564
110. Vogler I, Newrzela S, Hartmann S, Schneider N, Von Laer D, Koehl U, et al. An improved bicistronic CD20/tCD34 vector for efficient purification and in vivo depletion of gene-modified T cells for adoptive immunotherapy. Mol Ther (2010) 18:1330-8. doi:10.1038/mt.2010.83
111. Wang X, Chang WC, Wong CW, Colcher D, Sherman M, Ostberg JR, et al. A transgene-encoded cell surface polypeptide for selection, in vivo tracking, and ablation of engineered cells. Blood (2011) 118:1255-63. doi:10.1182/blood-2011-02-337360
112. Grupp SA, Kalos M, Barrett D, Aplenc R, Porter DL, Rheingold SR, et al. Chimeric antigen receptor-modified T cells for acute lymphoid leukemia. N Engl J Med (2013) 368:1509-18. doi:10.1056/NEJMoa1215134
113. Davila ML, Riviere I, Wang X, Bartido S, Park J, Curran K, et al. Efficacy and toxicity management of 19-28z CAR T cell therapy in B cell acute lymphoblastic leukemia. Sci Transl Med (2014) 6:224ra225. doi:10.1126/scitranslmed.3008226
114. Hudecek M, Schmitt TM, Baskar S, Lupo-Stanghellini MT, Nishida T, Yamamoto TN, et al. The B-cell tumor-associated antigen ROR1 can be targeted with T cells modified to express a ROR1-specific chimeric antigen receptor. Blood (2010) 116:4532-41. doi:10.1182/blood-2010-05-283309
115. Giordano Attianese GM, Marin V, Hoyos V, Savoldo B, Pizzitola I, Tettamanti S, et al. In vitro and in vivo model of a novel immunotherapy approach for chronic lymphocytic leukemia by anti-CD23 chimeric antigen receptor. Blood (2011) 117:4736-45. doi:10.1182/blood-2010-10-311845
116. Matsuki E, Younes A. Lymphomagenesis in Hodgkin lymphoma. Semin Cancer Biol (2015). doi:10.1016/j.semcancer.2015.02.002
117. Dave SS, Wright G, Tan B, Rosenwald A, Gascoyne RD, Chan WC, et al. Prediction of survival in follicular lymphoma based on molecular features of tumor-infiltrating immune cells. N Engl J Med (2004) 351:2159-69. doi:10.1056/NEJMoa041869
118. Lee AM, Clear AJ, Calaminici M, Davies AJ, Jordan S, Macdougall F, et al. Number of CD4+ cells and location of forkhead box protein P3-positive cells in diagnostic follicular lymphoma tissue microarrays correlates with outcome. J Clin Oncol (2006) 24:5052-9. doi:10.1200/JCO.2006.06.4642
119. Glas AM, Knoops L, Delahaye L, Kersten MJ, Kibbelaar RE, Wessels LA, et al. Gene-expression and immunohistochemical study of specific T-cell subsets and accessory cell types in the transformation and prognosis of follicular lymphoma. J Clin Oncol (2007) 25:390-8. doi:10.1200/JCO.2006.06.1648
120. Lenz G, Wright G, Dave SS, Xiao W, Powell J, Zhao H, et al. Stromal gene signatures in large-B-cell lymphomas. N Engl J Med (2008) 359:2313-23. doi:10.1056/NEJMoa0802885
121. Farinha P, Al-Tourah A, Gill K, Klasa R, Connors JM, Gascoyne RD. The architectural pattern of FOXP3-positive T cells in follicular lymphoma is an independent predictor of survival and histologic transformation. Blood (2010) 115:289-95. doi:10.1182/blood-2009-07-235598
122. Lin Y, Gustafson MP, Bulur PA, Gastineau DA, Witzig TE, Dietz AB. Immunosuppressive CD14+HLA-DR(low)/-monocytes in B-cell non-Hodgkin lymphoma. Blood (2011) 117:872-81. doi:10.1182/blood-2010-05-283820
123. Khalifa KA, Badawy HM, Radwan WM, Shehata MA, Bassuoni MA. CD14(+) HLA-DR low/(-) monocytes as indicator of disease aggressiveness in B-cell non-Hodgkin lymphoma. Int J Lab Hematol (2014) 36:650-5. doi:10.1111/ijlh.12203
124. 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
125. Met O, Wang M, Pedersen AE, Nissen MH, Buus S, Claesson MH. The effect of a therapeutic dendritic cell-based cancer vaccination depends on the blockage of CTLA-4 signaling. Cancer Lett (2006) 231:247-56. doi:10.1016/j.canlet.2005.02.005
126. Houot R, Levy R. T-cell modulation combined with intratumoral CpG cures lymphoma in a mouse model without the need for chemotherapy. Blood (2009) 113:3546-52. doi:10.1182/blood-2008-07-170274
127. Kohrt HE, Houot R, Goldstein MJ, Weiskopf K, Alizadeh AA, Brody J, et al. CD137 stimulation enhances the antilymphoma activity of anti-CD20 antibodies. Blood (2011) 117:2423-32. doi:10.1182/blood-2010-08-301945
128. Berger R, Rotem-Yehudar R, Slama G, Landes S, Kneller A, Leiba M, et al. Phase I safety and pharmacokinetic study of CT-011, a humanized antibody interacting with PD-1, in patients with advanced hematologic malignancies. Clin Cancer Res (2008) 14:3044-51. doi:10.1158/1078-0432.CCR-07-4079
129. 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) 15:6446-53. doi:10.1158/1078-0432.CCR-09-1339
130. Bashey A, Medina B, Corringham S, Pasek M, Carrier E, Vrooman L, et al. CTLA4 blockade with ipilimumab to treat relapse of malignancy after allogeneic hematopoietic cell transplantation. Blood (2009) 113:1581-8. doi:10.1182/blood-2008-07-168468
131. 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
132. Lin W, Voskens CJ, Zhang X, Schindler DG, Wood A, Burch E, et al. Fc-dependent expression of CD137 on human NK cells: insights into "agonistic" effects of anti-CD137 monoclonal antibodies. Blood (2008) 112:699-707. doi:10.1182/blood-2007-11-122465
133. Wiernik PH, Lossos IS, Tuscano JM, Justice G, Vose JM, Cole CE, et al. Lenalidomide monotherapy in relapsed or refractory aggressive non-Hodgkin's lymphoma. J Clin Oncol (2008) 26:4952-7. doi:10.1200/JCO.2007.15.3429
134. Habermann TM, Lossos IS, Justice G, Vose JM, Wiernik PH, Mcbride K, et al. Lenalidomide oral monotherapy produces a high response rate in patients with relapsed or refractory mantle cell lymphoma. Br J Haematol (2009) 145:344-9. doi:10.1111/j.1365-2141.2009.07626.x
135. Witzig TE, Wiernik PH, Moore T, Reeder C, Cole C, Justice G, et al. Lenalidomide oral monotherapy produces durable responses in relapsed or refractory indolent non-Hodgkin's Lymphoma. J Clin Oncol (2009) 27:5404-9. doi:10.1200/JCO.2008.21.1169
136. Witzig TE, Vose JM, Zinzani PL, Reeder CB, Buckstein R, Polikoff JA, et al. An international phase II trial of single-agent lenalidomide for relapsed or refractory aggressive B-cell non-Hodgkin's lymphoma. Ann Oncol (2011) 22:1622-7. doi:10.1093/annonc/mdq626
137. Goy A, Sinha R, Williams ME, Kalayoglu Besisik S, Drach J, Ramchandren R, et al. Single-agent lenalidomide in patients with mantle-cell lymphoma who relapsed or progressed after or were refractory to bortezomib: phase II MCL-001 (EMERGE) study. J Clin Oncol (2013) 31:3688-95. doi:10.1200/JCO.2013.49.2835
138. Zinzani PL, Pellegrini C, Gandolfi L, Stefoni V, Quirini F, Derenzini E, et al. Combination of lenalidomide and rituximab in elderly patients with relapsed or refractory diffuse large B-cell lymphoma: a phase 2 trial. Clin Lymphoma Myeloma Leuk (2011) 11:462-6. doi:10.1016/j.clml.2011.02.001
139. Tuscano JM, Dutia M, Chee K, Brunson A, Reed-Pease C, Abedi M, et al. Lenalidomide plus rituximab can produce durable clinical responses in patients with relapsed or refractory, indolent non-Hodgkin lymphoma. Br J Haematol (2014) 165:375-81. doi:10.1111/bjh.12755
140. Plosker GL, Figgitt DP. Rituximab: a review of its use in non-Hodgkin's lymphoma and chronic lymphocytic leukaemia. Drugs (2003) 63:803-43. doi:10.2165/00003495-200363080-00005
141. Nowakowski GS, Laplant B, Habermann TM, Rivera CE, Macon WR, Inwards DJ, et al. Lenalidomide can be safely combined with R-CHOP (R2CHOP) in the initial chemotherapy for aggressive B-cell lymphomas: phase I study. Leukemia (2011) 25:1877-81. doi:10.1038/leu.2011.165
142. Vitolo U, Chiappella A, Franceschetti S, Carella AM, Baldi I, Inghirami G, et al. Lenalidomide plus R-CHOP21 in elderly patients with untreated diffuse large B-cell lymphoma: results of the REAL07 open-label, multicentre, phase 2 trial. Lancet Oncol (2014) 15:730-7. doi:10.1016/S1470-2045(14)70191-3
143. Nowakowski GS, Laplant B, Macon WR, Reeder CB, Foran JM, Nelson GD, et al. Lenalidomide combined with R-CHOP overcomes negative prognostic impact of non-germinal center B-cell phenotype in newly diagnosed diffuse large B-Cell lymphoma: a phase II study. J Clin Oncol (2015) 33:251-7. doi:10.1200/JCO.2014.55.5714