Novel targeted agents in hodgkin and non-hodgkin lymphoma therapy

Pharmaceuticals

Volumn 8, Issue 3, 2015, Pages 607-636

  Grover, Natalie S ^a   Park, Steven I ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Antibody drug conjugates; Hodgkin lymphoma; Immune checkpoint inhibitors; Monoclonal antibody; Non Hodgkin lymphoma; Small molecule inhibitors

Indexed keywords

ANTIBODY CONJUGATE; ANTINEOPLASTIC AGENT; BLINATUMOMAB; BRENTUXIMAB VEDOTIN; COLTUXIMAB RAVTANSINE; CYCLOPHOSPHAMIDE; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; DENINTUZUMAB MAFODOTIN; DOXORUBICIN; DUVELISIB; EPRATUZUMAB; IBRUTINIB; IDELALISIB; INEBILIZUMAB; INOTUZUMAB OZOGAMICIN; IPILIMUMAB; LUCATUMUMAB; MEMBRANE ANTIGEN; NIVOLUMAB; OBINUTUZUMAB; OFATUMUMAB; PEMBROLIZUMAB; PHOSPHOTRANSFERASE INHIBITOR; PIDILIZUMAB; POLATUZUMAB VEDOTIN; PREDNISONE; PROGRAMMED DEATH 1 RECEPTOR; RITUXIMAB; UNINDEXED DRUG; VINCRISTINE;

ABNORMAL LABORATORY RESULT; ACUTE LYMPHOBLASTIC LEUKEMIA; ADVANCED CANCER; ANEMIA; ANTIGEN ANTIBODY REACTION; ANTINEOPLASTIC ACTIVITY; B CELL LYMPHOMA; BLOOD TOXICITY; BLURRED VISION; BRAIN DISEASE; CANCER CHEMOTHERAPY; CANCER SURVIVAL; CHILL; CHRONIC LYMPHATIC LEUKEMIA; CLINICAL TRIAL (TOPIC); COLITIS; CONFUSION; CORNEA DISEASE; CYTOPENIA; DIARRHEA; DRUG APPROVAL; DRUG EFFICACY; DRUG FEVER; DRUG MECHANISM; DRUG SAFETY; DRUG TARGETING; DRUG TOLERABILITY; FOLLICULAR LYMPHOMA; HEMATOLOGIC MALIGNANCY; HODGKIN DISEASE; HUMAN; HYPERTRANSAMINASEMIA; INFECTION; INFUSION RELATED REACTION; LARGE CELL LYMPHOMA; LEUKOPENIA; LIVER TOXICITY; LYMPHOCYTOPENIA; MANTLE CELL LYMPHOMA; MULTIPLE MYELOMA; MYELODYSPLASTIC SYNDROME; NEUROPATHY; NEUTROPENIA; NONHODGKIN LYMPHOMA; NONHUMAN; OUTCOME ASSESSMENT; OVERALL SURVIVAL; PANCREATITIS; PERIPHERAL NEUROPATHY; PERIPHERAL T CELL LYMPHOMA; PNEUMONIA; PROGRESSION FREE SURVIVAL; RESPIRATORY TRACT DISEASE; REVIEW; SENSORY NEUROPATHY; SOLID TUMOR; SPEECH DISORDER; STOMATITIS; T CELL LYMPHOMA; THROMBOCYTOPENIA; THYROID DISEASE; TREATMENT RESPONSE; TREMOR;

EID: 84941958587     PISSN: None     EISSN: 14248247     Source Type: Journal    
DOI: 10.3390/ph8030607     Document Type: Review

References (112)

1. Siegel, R.L.; Miller, K.D.; Jemal, A. Cancer Statistics, 2015. CA Cancer J. Clin. 2015, 65, 5-29.
2. Fisher, R.I.; Gaynor, E.R.; Dahlberg, S.; Oken, M.M.; Grogan, T.M.; Mize, E.M.; Glick, J.H.; Coltman, C.A., Jr.; Miller, T.P. Comparison of a standard regimen (CHOP) with three intensive chemotherapy regimens for advanced non-Hodgkin's lymphoma. N. Engl. J. Med. 1993, 328, 1002-1006.
3. Sehn, L.H.; Donaldson, J.; Chhanabhai, M.; Fitzgerald, C.; Gill, K.; Klasa, R.; MacPherson, N.; O'Reilly, S.; Spinelli, J.J.; Sutherland, J.; et al. Introduction of combined CHOP plus rituximab therapy dramatically improved outcome of diffuse large B-cell lymphoma in British Columbia. J. Clin. Oncol. 2005, 23, 5027-5033.
4. Cheson, B.D.; Leonard, J.P. Monoclonal antibody therapy for B-cell non-Hodgkin's lymphoma. N. Engl. J. Med. 2008, 359, 613-626.
5. Mossner, E.; Brunker, P.; Moser, S.; Puntener, U.; Schmidt, C.; Herter, S.; Grau, R.; Gerdes, C.; Nopora, A.; van Puijenbroek, E.; et al. Increasing the efficacy of CD20 antibody therapy through the engineering of a new type II anti-CD20 antibody with enhanced direct and immune effector cell-mediated B-cell cytotoxicity. Blood 2010, 115, 4393-4402.
6. Alduaij, W.; Ivanov, A.; Honeychurch, J.; Cheadle, E.J.; Potluri, S.; Lim, S.H.; Shimada, K.; Chan, C.H.; Tutt, A.; Beers, S.A.; et al. Novel type II anti-CD20 monoclonal antibody (GA101) evokes homotypic adhesion and actin-dependent, lysosome-mediated cell death in B-cell malignancies. Blood 2011, 117, 4519-4529.
7. Salles, G.; Morschhauser, F.; Lamy, T.; Milpied, N.; Thieblemont, C.; Tilly, H.; Bieska, G.; Asikanius, E.; Carlile, D.; Birkett, J.; et al. Phase 1 study results of the type II glycoengineered humanized anti-CD20 monoclonal antibody obinutuzumab (GA101) in B-cell lymphoma patients. Blood 2012, 119, 5126-5132.
8. Sehn, L.H.; Assouline, S.E.; Stewart, D.A.; Mangel, J.; Gascoyne, R.D.; Fine, G.; Frances-Lasserre, S.; Carlile, D.J.; Crump, M. A Phase 1 study of obinutuzumab induction followed by 2 years of maintenance in patients with relapsed CD20-positive B-cell malignancies. Blood 2012, 119, 5118-5125.
9. Salles, G.A.; Morschhauser, F.; Solal-Celigny, P.; Thieblemont, C.; Lamy, T.; Tilly, H.; Gyan, E.; Lei, G.; Wenger, M.; Wassner-Fritsch, E.; et al. Obinutuzumab (GA101) in patients with relapsed/refractory indolent non-Hodgkin lymphoma: Results from the phase II GAUGUIN study. J. Clin. Oncol. 2013, 31, 2920-2926.
10. Morschhauser, F.A.; Cartron, G.; Thieblemont, C.; Solal-Celigny, P.; Haioun, C.; Bouabdallah, R.; Feugier, P.; Bouabdallah, K.; Asikanius, E.; Lei, G.; et al. Obinutuzumab (GA101) monotherapy in relapsed/refractory diffuse large B-cell lymphoma or mantle-cell lymphoma: Results from the phase II GAUGUIN study. J. Clin. Oncol. 2013, 31, 2912-2919.
11. Radford, J.; Davies, A.; Cartron, G.; Morschhauser, F.; Salles, G.; Marcus, R.; Wenger, M.; Lei, G.; Wassner-Fritsch, E.; Vitolo, U. Obinutuzumab (GA101) plus CHOP or FC in relapsed/refractory follicular lymphoma: Results of the GAUDI study (BO21000). Blood 2013, 122, 1137-1143.
12. Dyer, M.J.; Grigg, A.P.; González Díaz, M.; Dreyling, M.; Rule, S.; Lei, G.; Wassner-Fritsch, E.; Fingerle-Rowson, G.; Marlton, P.V. Obinutuzumab (GA101) in combination with CHOP (cyclophosphamide, doxorubicin, vincristine and prednisone) or bendamustine for the first-line treatment of follicular non-Hodgkin lymphoma: Final results from the maintenance phase of the phase Ib GAUDI study. Blood 2014, 124, 1743-1743.
13. Sehn, L.H.; Chua, N.S.; Mayer, J.; Dueck, G.S.; Trněny, M.; Bouabdallah, K.; Fowler, N.H.; Delwail, V.; Press, O.W.; Salles, G.A.; et al. GADOLIN: Primary results from a phase III study of obinutuzumab plus bendamustine compared with bendamustine alone in patients with rituximab-refractory indolent non-Hodgkin lymphoma. J. Clin. Oncol. (ASCO Meeting Abstracts) 2015, 33, Abstract LBA8502.
14. Sehn, L.H.; Goy, A.; Offner, F.C.; Martinelli, G.; Friedberg, J.; Lasserre, S.F.; Fine, G.; Press, O.W. Randomized phase II trial comparing GA101 (obinutuzumab) with rituximab in patients with relapsed CD20 indolent B-cell non-Hodgkin lymphoma: Preliminary analysis of the GAUSS study. Blood (ASH Annual Meeting Abstracts), 2011, 118, Abstract 269.
15. Goede, V.; Fischer, K.; Busch, R.; Engelke, A.; Eichhorst, B.; Wendtner, C.M.; Chagorova, T.; de la Serna, J.; Dilhuydy, M.S.; Illmer, T.; et al. Obinutuzumab with CLL and coexisting conditions. N. Engl. J. Med. 2014, 370, 1101-1110.
16. Teeling, J.L.; French, R.R.; Cragg, M.S.; van den Brakel, J.; Pluyter, M.; Huang, H.; Chan, C.; Parren, P.W.; Hack, C.E.; Dechant, M.; et al. Characterization of new human CD20 monoclonal antibodies with potent cytolytic activity against non-Hodgkin lymphomas. Blood 2004, 104, 1793-1800.
17. Pawluczkowycz, A.W.; Beurskens, F.J.; Beum, P.V.; Lindorfer, M.A.; van de Winkel, J.G.; Parren, P.W.; Taylor, R.P. Binding of submaximal C1q promotes complement-dependent cytotoxicity (CDC) of B cells opsonized with anti-CD20 mAbs ofatumumab (OFA) or rituximab (RTX): Considerably higher levels of CDC are induced by ofa than by RTX. J. Immunol. 2009, 183, 749-758.
18. Coiffier, B.; Lepretre, S.; Pedersen, L.M.; Gadeberg, O.; Fredriksen, H.; van Oers, M.H.; Wooldridge, J.; Kloczko, J.; Holowiecki, J.; Hellmann, A.; et al. Safety and efficacy of ofatumumab, a fully human monoclonal anti-CD20 antibody, in patients with relapsed or refractory B-cell chronic lymphocytic leukemia: A phase 1-2 study. Blood 2008, 111, 1094-1100.
19. Wierda, W.G.; Kipps, T.J.; Mayer, J.; Stilgenbauer, S.; Williams, C.D.; Hellmann, A.; Robak, T.; Furman, R.R.; Hillmen, P.; Trneny, M.; et al. Ofatumumab as single-agent CD20 immunotherapy in fludarabine-refractory chronic lymphocytic leukemia. J. Clin. Oncol. 2010, 28, 1749-1755.
20. Hillmen, P.; Robak, T.; Janssens, A.; Babu, K.G.; Kloczko, J.; Grosicki, S.; Doubek, M.; Panagiotidis, P.; Kimby, E.; Schuh, A.; et al. Chlorambucil plus ofatumumab versus chlorambucil alone in previously untreated patients with chronic lymphocytic leukaemia (COMPLEMENT 1): A randomised, multicentre, open-label phase 3 trial. Lancet 2015, 385, 1873-1883.
21. Hagenbeek, A.; Gadeberg, O.; Johnson, P.; Pedersen, L.M.; Walewski, J.; Hellmann, A.; Link, B.K.; Robak, T.; Wojtukiewicz, M.; Pfreundschuh, M.; et al. First clinical use of ofatumumab, a novel fully human anti-CD20 monoclonal antibody in relapsed or refractory follicular lymphoma: Results of a phase 1/2 trial. Blood 2008, 111, 5486-5495.
22. Czuczman, M.S.; Fayad, L.; Delwail, V.; Cartron, G.; Jacobsen, E.; Kuliczkowski, K.; Link, B.K.; Pinter-Brown, L.; Radford, J.; Hellmann, A.; et al. Ofatumumab monotherapy in rituximab-refractory follicular lymphoma: Results from a multicenter study. Blood 2012, 119, 3698-3704.
23. Czuczman, M.S.; Hess, G.; Gadeberg, O.V.; Pedersen, L.M.; Goldstein, N.; Gupta, I.; Jewell, R.C.; Lin, T.S.; Lisby, S.; Strange, C.; et al. Chemoimmunotherapy with ofatumumab in combination with CHOP in previously untreated follicular lymphoma. Br. J. Haematol. 2012, 157, 438-445.
24. Czuczman, M.S.; Kahanic, S.; Forero, A.; Davis, G.; Munteanu, M.; Van Den Neste, E.; Offner, F.; Bron, D.; Quick, D.; Fowler, N. Results of a phase II study of bendamustine and ofatumumab in untreated indolent B cell non-Hodgkin's lymphoma. Ann. Hematol. 2015, 94, 633-641.
25. Van Imhoff, G.W.; McMillan, A.; Matasar, M.J.; Radford, J.; Ardeshna, K.M.; Kuliczkowski, K.; Kim, W.; Hong, X.; Soenderskov Goerloev, J.; Davies, A.; et al. Ofatumumab versus rituximab salvage chemoimmunotherapy in relapsed or refractory diffuse large B-cell lymphoma: The orcharrd study (OMB110928). Blood 2014, 124, 630-630.
26. Merli, M.; Ferrario, A.; Maffioli, M.; Arcaini, L.; Passamonti, F. Investigational therapies targeting lymphocyte antigens for the treatment of non-Hodgkin's lymphoma. Expert Opin. Investig. Drugs 2015, 24, 897-912.
27. Kumar, A.; Younes, A. Role of CD30 targeting in malignant lymphoma. Curr. Treat. Options Oncol. 2014, 15, 210-225.
28. Francisco, J.A.; Cerveny, C.G.; Meyer, D.L.; Mixan, B.J.; Klussman, K.; Chace, D.F.; Rejniak, S.X.; Gordon, K.A.; DeBlanc, R.; Toki, B.E.; et al. cAC10-vcMMAE, an anti-CD30-monomethyl auristatin E conjugate with potent and selective antitumor activity. Blood 2003, 102, 1458-1465.
29. Majhail, N.S.; Weisdorf, D.J.; Defor, T.E.; Miller, J.S.; McGlave, P.B.; Slungaard, A.; Arora, M.; Ramsay, N.K.; Orchard, P.J.; MacMillan, M.L.; et al. Long-term results of autologous stem cell transplantation for primary refractory or relapsed Hodgkin's lymphoma. Biol. Blood Marrow Transplant. 2006, 12, 1065-1072.
30. Merkel, O.; Hamacher, F.; Sifft, E.; Kenner, L.; Greil, R. Novel therapeutic options in anaplastic large cell lymphoma: Molecular targets and immunological tools. Mol. Cancer. Ther. 2011, 10, 1127-1136.
31. Younes, A.; Bartlett, N.L.; Leonard, J.P.; Kennedy, D.A.; Lynch, C.M.; Sievers, E.L.; Forero-Torres, A. Brentuximab vedotin (SGN-35) for relapsed CD30-positive lymphomas. N. Engl. J. Med. 2010, 363, 1812-1821.
32. Younes, A.; Gopal, A.K.; Smith, S.E.; Ansell, S.M.; Rosenblatt, J.D.; Savage, K.J.; Ramchandren, R.; Bartlett, N.L.; Cheson, B.D.; de Vos, S.; et al. Results of a pivotal phase II study of brentuximab vedotin for patients with relapsed or refractory Hodgkin's lymphoma. J. Clin. Oncol. 2012, 30, 2183-2189.
33. Younes, A.; Connors, J.M.; Park, S.I.; Fanale, M.; O'Meara, M.M.; Hunder, N.N.; Huebner, D.; Ansell, S.M. Brentuximab vedotin combined with ABVD Or AVD for patients with newly diagnosed Hodgkin's lymphoma: A phase 1, open-label, dose-escalation study. Lancet Oncol. 2013, 14, 1348-1356.
34. Pro, B.; Advani, R.; Brice, P.; Bartlett, N.L.; Rosenblatt, J.D.; Illidge, T.; Matous, J.; Ramchandren, R.; Fanale, M.; Connors, J.M.; et al. Brentuximab vedotin (SGN-35) in patients with relapsed or refractory systemic anaplastic large-cell lymphoma: Results of a phase II study. J. Clin. Oncol. 2012, 30, 2190-2196.
35. Pro, B.; Advani, R.; Brice, P.; Bartlett, N.L.; Rosenblatt, J.D.; Illidge, T.; Matous, J.; Ramchandern, R.; Fanale, M.A.; Connors, J.M.; et al. Four-year survival data from an ongoing pivotal phase 2 study of brentuximab vedotin in patients with relapsed or refractory systemic anaplastic large cell lymphoma. Blood 2014, 124, 3095-3095.
36. Fanale, M.A.; Horwitz, S.M.; Forero-Torres, A.; Bartlett, N.L.; Advani, R.H.; Pro, B.; Chen, R.W.; Davies, A.; Illidge, T.; Huebner, D.; et al. Brentuximab vedotin in the front-line treatment of patients with CD30+ peripheral T-cell lymphomas: Results of a phase I study. J. Clin. Oncol. 2014, 32, 3137-3143.
37. Horwitz, S.M.; Advani, R.H.; Bartlett, N.L.; Jacobsen, E.D.; Sharman, J.P.; O'Connor, O.A.; Siddiqi, T.; Kennedy, D.A.; Oki, Y. Objective responses in relapsed T-cell lymphomas with single-agent brentuximab vedotin. Blood 2014, 123, 3095-3100.
38. Bartlett, N.L.; Farber, C.M.; Yasenchak, C.A.; Ansell, S.M.; Advani, R.H.; Knapp, M.H.; Fayad, L.; Kolibaba, K.S.; Patel-Donnelly, D.; Seetharam, M.; et al. Updated results of a phase II trial of brentuximab vedotin combined with R-CHOP in frontline treatment of patients (Pts) with high-intermediate/high-risk diffuse large B-cell lymphoma (DLBCL). J. Clin. Oncol. (ASCO Meeting Abstracts) 2015, 33, Abstract 8506.
39. Palanca-Wessels, M.C.; Czuczman, M.; Salles, G.; Assouline, S.; Sehn, L.H.; Flinn, I.; Patel, M.R.; Sangha, R.; Hagenbeek, A.; Advani, R.; et al. Safety and activity of the anti-CD79B antibody-drug conjugate polatuzumab vedotin in relapsed or refractory B-cell non-Hodgkin lymphoma and chronic lymphocytic leukaemia: A phase 1 study. Lancet Oncol. 2015, 16, 704-715.
40. Leonard, J.P.; Coleman, M.; Ketas, J.C.; Chadburn, A.; Furman, R.; Schuster, M.W.; Feldman, E.J.; Ashe, M.; Schuster, S.J.; Wegener, W.A.; et al. Epratuzumab, a humanized anti-CD22 antibody, in aggressive non-Hodgkin's lymphoma: Phase I/II clinical trial results. Clin. Cancer Res. 2004, 10, 5327-5334.
41. Leonard, J.P.; Coleman, M.; Ketas, J.; Ashe, M.; Fiore, J.M.; Furman, R.R.; Niesvizky, R.; Shore, T.; Chadburn, A.; Horne, H.; et al. Combination antibody therapy with epratuzumab and rituximab in relapsed or refractory non-Hodgkin's lymphoma. J. Clin. Oncol. 2005, 23, 5044-5051.
42. Strauss, S.J.; Morschhauser, F.; Rech, J.; Repp, R.; Solal-Celigny, P.; Zinzani, P.L.; Engert, A.; Coiffier, B.; Hoelzer, D.F.; Wegener, W.A.; et al. Multicenter phase II trial of immunotherapy with the humanized anti-CD22 antibody, epratuzumab, in combination with rituximab, in refractory or recurrent non-Hodgkin's lymphoma. J. Clin. Oncol. 2006, 24, 3880-3886.
43. Micallef, I.N.; Maurer, M.J.; Wiseman, G.A.; Nikcevich, D.A.; Kurtin, P.J.; Cannon, M.W.; Perez, D.G.; Soori, G.S.; Link, B.K.; Habermann, T.M.; et al. Epratuzumab with rituximab, cyclophosphamide, doxorubicin, vincristine, and prednisone chemotherapy in patients with previously untreated diffuse large B-cell lymphoma. Blood 2011, 118, 4053-4061.
44. Advani, A.; Coiffier, B.; Czuczman, M.S.; Dreyling, M.; Foran, J.; Gine, E.; Gisselbrecht, C.; Ketterer, N.; Nasta, S.; Rohatiner, A.; et al. Safety, pharmacokinetics, and preliminary clinical activity of inotuzumab ozogamicin, a novel immunoconjugate for the treatment of B-cell non-Hodgkin's lymphoma: Results of a phase I study. J. Clin. Oncol. 2010, 28, 2085-2093.
45. Fayad, L.; Offner, F.; Smith, M.R.; Verhoef, G.; Johnson, P.; Kaufman, J.L.; Rohatiner, A.; Advani, A.; Foran, J.; Hess, G.; et al. Safety and clinical activity of a combination therapy comprising two antibody-based targeting agents for the treatment of non-Hodgkin lymphoma: results of a phase I/II Study evaluating the immunoconjugate inotuzumab ozogamicin with rituximab. J. Clin. Oncol. 2013, 31, 573-583.
46. Shor, B.; Gerber, H.P.; Sapra, P. Preclinical and clinical development of inotuzumab-ozogamicin in hematological malignancies. Mol. Immunol. 2015, 67, 107-116.
47. Fanale, M.; Assouline, S.; Kuruvilla, J.; Solal-Celigny, P.; Heo, D.S.; Verhoef, G.; Corradini, P.; Abramson, J.S.; Offner, F.; Engert, A.; et al. Phase IA/II, multicentre, open-label study of the CD40 antagonistic monoclonal antibody lucatumumab in adult patients with advanced non-Hodgkin or Hodgkin lymphoma. Br. J. Haematol. 2014, 164, 258-265.
48. Hamadani, M.; Fanale, M.A.; Bello, C.M.; Kipps, T.J.; Offner, F.; Verhoef, G.; Federico, M.; Gregory, S.A.; Sonet, A.; Assouline, S.; et al. Safety profile and clinical response to MEDI-551, a humanized monoclonal anti-CD19, in a phase 1/2 study in adults with relapsed or refractory advanced B-cell malignancies. Blood 2013, 122, 1810-1810.
49. Ogura, M.; Ando, K.; Uike, N.; Ogawa, Y.; Uchida, T.; Abe, Y.; Morishita, T.; Kojima, M.; Choi, I.; Yagawa, K.; et al. A multicenter phase I study of the humanized anti-CD19 monoclonal antibody, MEDI-551, in patients with relapsed or refractory B-cell lymphoma and multiple myeloma. Blood 2014, 124, 1756-1756.
50. Raufi, A.; Ebrahim, A.S.; Al-Katib, A. Targeting CD19 in B-cell lymphoma: Emerging role of SAR3419. Cancer. Manag. Res. 2013, 5, 225-233.
51. Younes, A.; Kim, S.; Romaguera, J.; Copeland, A.; Farial Sde, C.; Kwak, L.W.; Fayad, L.; Hagemeister, F.; Fanale, M.; Neelapu, S.; et al. Phase I multidose-escalation study of the anti-CD19 maytansinoid immunoconjugate SAR3419 administered by intravenous infusion every 3 weeks to patients with relapsed/refractory B-cell lymphoma. J. Clin. Oncol. 2012, 30, 2776-2782.
52. Ribrag, V.; Dupuis, J.; Tilly, H.; Morschhauser, F.; Laine, F.; Houot, R.; Haioun, C.; Copie, C.; Varga, A.; Lambert, J.; et al. A dose-escalation study of SAR3419, an anti-CD19 antibody maytansinoid conjugate, administered by intravenous infusion once weekly in patients with relapsed/refractory B-cell non-Hodgkin lymphoma. Clin. Cancer Res. 2014, 20, 213-220.
53. Moskowitz, C.H.; Forero-Torres, A.; Shah, B.D.; Advani, R.; Hamlin, P.; Kim, S.; Kostic, A.; Sandalic, L.; Zhao, B.; Fanale, M.A. Interim analysis of a phase 1 study of the antibody-drug conjugate SGN-CD19A in relapsed or refractory B-lineage non-Hodgkin lymphoma. Blood 2014, 124, 1741-1741.
54. Loffler, A.; Kufer, P.; Lutterbuse, R.; Zettl, F.; Daniel, P.T.; Schwenkenbecher, J.M.; Riethmuller, G.; Dorken, B.; Bargou, R.C. A Recombinant bispecific single-chain antibody, CD19 × CD3, induces rapid and high lymphoma-directed cytotoxicity by unstimulated T lymphocytes. Blood 2000, 95, 2098-2103.
55. Bargou, R.; Leo, E.; Zugmaier, G.; Klinger, M.; Goebeler, M.; Knop, S.; Noppeney, R.; Viardot, A.; Hess, G.; Schuler, M.; et al. Tumor regression in cancer patients by very low doses of a T cell-engaging antibody. Science 2008, 321, 974-977.
56. Viardot, A.; Goebeler, M.; Hess, G.; Neumann, S.; Pfreundschuh, M.; Adrian, N.; Zettl, F.; Libicher, M.; Degenhard, E.; Stieglmaier, J.; et al. Treatment of relapsed/refractory diffuse large B-cell lymphoma with the bispecific T-cell engager (BiTE®) antibody construct blinatumomab: Primary analysis results from an open-label, phase 2 study. Blood 2014, 124, 4460-4460.
57. Topp, M.S.; Gokbuget, N.; Stein, A.S.; Zugmaier, G.; O'Brien, S.; Bargou, R.C.; Dombret, H.; Fielding, A.K.; Heffner, L.; Larson, R.A.; et al. Safety and activity of blinatumomab for adult patients with relapsed or refractory B-precursor acute lymphoblastic leukaemia: A multicentre, single-arm, phase 2 study. Lancet Oncol. 2015, 16, 57-66.
58. Ansell, S.M.; Hurvitz, S.A.; Koenig, P.A.; LaPlant, B.R.; Kabat, B.F.; Fernando, D.; Habermann, T.M.; Inwards, D.J.; Verma, M.; Yamada, R.; 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.
59. Armand, P. Immune checkpoint blockade in hematologic malignancies. Blood 2015, 125, 3393-3400.
60. Green, M.R.; Monti, S.; Rodig, S.J.; Juszczynski, P.; Currie, T.; O'Donnell, E.; Chapuy, B.; Takeyama, K.; Neuberg, D.; Golub, T.R.; 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.
61. Green, M.R.; Rodig, S.; Juszczynski, P.; Ouyang, J.; Sinha, P.; O'Donnell, E.; Neuberg, D.; Shipp, M.A. 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, 1611-1618.
62. Prieto, P.A.; Yang, J.C.; Sherry, R.M.; Hughes, M.S.; Kammula, U.S.; White, D.E.; Levy, C.L.; Rosenberg, S.A.; Phan, G.Q. CTLA-4 blockade with ipilimumab: Long-term follow-up of 177 patients with metastatic melanoma. Clin. Cancer Res. 2012, 18, 2039-2047.
63. Berger, R.; Rotem-Yehudar, R.; Slama, G.; Landes, S.; Kneller, A.; Leiba, M.; Koren-Michowitz, M.; Shimoni, A.; Nagler, A. 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, 3044-3051.
64. Armand, P.; Nagler, A.; Weller, E.A.; Devine, S.M.; Avigan, D.E.; Chen, Y.B.; Kaminski, M.S.; Holland, H.K.; Winter, J.N.; Mason, J.R.; 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.
65. Westin, J.R.; Chu, F.; Zhang, M.; Fayad, L.E.; Kwak, L.W.; Fowler, N.; Romaguera, J.; Hagemeister, F.; Fanale, M.; Samaniego, F.; 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.
66. Ansell, S.M.; Lesokhin, A.M.; Borrello, I.; Halwani, A.; Scott, E.C.; Gutierrez, M.; Schuster, S.J.; Millenson, M.M.; Cattry, D.; Freeman, G.J.; et al. PD-1 blockade with nivolumab in relapsed or refractory Hodgkin's lymphoma. N. Engl. J. Med. 2015, 372, 311-319.
67. Lesokhin, A.M.; Ansell, S.M.; Armand, P.; Scott, E.C.; Halwani, A.; Gutierrez, M.; Millenson, M.M.; Cohen, A.D.; Schuster, S.J.; Lebovic, D.; et al. Preliminary results of a phase I study of nivolumab (BMS-936558) in patients with relapsed or refractory lymphoid malignancies. Blood 2014, 124, 291-291.
68. Moskowitz, C.H.; Ribrag, V.; Michot, J.; Martinelli, G.; Zinzani, P.L.; Gutierrez, M.; De Maeyer, G.; Jacob, A.G.; Giallella, K.; Weimer Anderson, J.; et al. PD-1 blockade with the monoclonal antibody pembrolizumab (MK-3475) in patients with classical hodgkin lymphoma after brentuximab vedotin failure: Preliminary results from a phase 1b study (KEYNOTE-013). Blood 2014, 124, 290-290.
69. Advani, R.H.; Buggy, J.J.; Sharman, J.P.; Smith, S.M.; Boyd, T.E.; Grant, B.; Kolibaba, K.S.; Furman, R.R.; Rodriguez, S.; Chang, B.Y.; et al. Bruton tyrosine kinase inhibitor ibrutinib (PCI-32765) has significant activity in patients with relapsed/refractory B-cell malignancies. J. Clin. Oncol. 2013, 31, 88-94.
70. Brown, J.R.; Byrd, J.C.; Coutre, S.E.; Benson, D.M.; Flinn, I.W.; Wagner-Johnston, N.D.; Spurgeon, S.E.; Kahl, B.S.; Bello, C.; Webb, H.K.; et al. Idelalisib, an inhibitor of phosphatidylinositol 3-kinase p110δ, for relapsed/refractory chronic lymphocytic leukemia. Blood 2014, 123, 3390-3397.
71. Flinn, I.W.; Kahl, B.S.; Leonard, J.P.; Furman, R.R.; Brown, J.R.; Byrd, J.C.; Wagner-Johnston, N.D.; Coutre, S.E.; Benson, D.M.; Peterman, S.; et al. Idelalisib, a selective inhibitor of phosphatidylinositol 3-kinase-delta, as therapy for previously treated indolent non-Hodgkin lymphoma. Blood 2014, 123, 3406-3413.
72. Younes, A.; Romaguera, J.; Fanale, M.; McLaughlin, P.; Hagemeister, F.; Copeland, A.; Neelapu, S.; Kwak, L.; Shah, J.; de Castro Faria, S.; et al. Phase I study of a novel oral janus kinase 2 inhibitor, SB1518, in patients with relapsed lymphoma: Evidence of clinical and biologic activity in multiple lymphoma subtypes. J. Clin. Oncol. 2012, 30, 4161-4167.
73. Chonghaile, T.N.; Letai, A. Mimicking the BH3 domain to kill cancer cells. Oncogene 2008, 27, S149-S157.
74. Roberts, A.W.; Seymour, J.F.; Brown, J.R.; Wierda, W.G.; Kipps, T.J.; Khaw, S.L.; Carney, D.A.; He, S.Z.; Huang, D.C.; Xiong, H.; et al. Substantial susceptibility of chronic lymphocytic leukemia to BCL2 inhibition: results of a phase I study of navitoclax in patients with relapsed or refractory disease. J. Clin. Oncol. 2012, 30, 488-496.
75. Kelly, K.R.; Shea, T.C.; Goy, A.; Berdeja, J.G.; Reeder, C.B.; McDonagh, K.T.; Zhou, X.; Danaee, H.; Liu, H.; Ecsedy, J.A.; et al. Phase I study of MLN8237-investigational aurora a kinase inhibitor-in relapsed/refractory multiple myeloma, non-Hodgkin lymphoma and chronic lymphocytic leukemia. Invest. New Drugs 2014, 32, 489-499.
76. Yakushijin, Y.; Hamada, M.; Yasukawa, M. The expression of the aurora-A gene and its significance with tumorgenesis in non-Hodgkin's lymphoma. Leuk. Lymphoma 2004, 45, 1741-1746.
77. Wang, X.; Zhou, Y.X.; Qiao, W.; Tominaga, Y.; Ouchi, M.; Ouchi, T.; Deng, C.X. Overexpression of aurora kinase A in mouse mammary epithelium induces genetic instability preceding mammary tumor formation. Oncogene 2006, 25, 7148-7158.
78. Hilton, J.F.; Shapiro, G.I. Aurora kinase inhibition as an anticancer strategy. J. Clin. Oncol. 2014, 32, 57-59.
79. Wang, M.L.; Rule, S.; Martin, P.; Goy, A.; Auer, R.; Kahl, B.S.; Jurczak, W.; Advani, R.H.; Romaguera, J.E.; Williams, M.E.; et al. Targeting BTK with ibrutinib in relapsed or refractory mantle-cell lymphoma. N. Engl. J. Med. 2013, 369, 507-516.
80. Byrd, J.C.; Furman, R.R.; Coutre, S.E.; Flinn, I.W.; Burger, J.A.; Blum, K.A.; Grant, B.; Sharman, J.P.; Coleman, M.; Wierda, W.G.; et al. Targeting BTK with ibrutinib in relapsed chronic lymphocytic leukemia. N. Engl. J. Med. 2013, 369, 32-42.
81. Byrd, J.C.; Brown, J.R.; O'Brien, S.; Barrientos, J.C.; Kay, N.E.; Reddy, N.M.; Coutre, S.; Tam, C.S.; Mulligan, S.P.; Jaeger, U.; et al. Ibrutinib versus ofatumumab in previously treated chronic lymphoid leukemia. N. Engl. J. Med. 2014, 371, 213-223.
82. Nowakowski, G.S.; Czuczman, M.S. ABC, GCB, and double-hit diffuse large B-cell lymphoma: Does subtype make a difference in therapy selection? Am. Soc. Clin. Oncol. Educ. Book 2015, 35, e449-e457.
83. Davis, R.E.; Ngo, V.N.; Lenz, G.; Tolar, P.; Young, R.M.; Romesser, P.B.; Kohlhammer, H.; Lamy, L.; Zhao, H.; Yang, Y.; et al. Chronic active B-cell-receptor signalling in diffuse large B-cell lymphoma. Nature 2010, 463, 88-92.
84. Young, R.M.; Staudt, L.M. Targeting pathological B cell receptor signalling in lymphoid malignancies. Nat. Rev. Drug Discov. 2013, 12, 229-243.
85. Wilson, W.H.; Gerecitano, J.F.; Goy, A.; de Vos, S.; Kenkre, V.P.; Barr, P.M.; Blum, K.A.; Shustov, A.R.; Advani, R.H.; Lih, J.; et al. The Bruton's tyrosine kinase (BTK) inhibitor, ibrutinib (PCI-32765), has preferential activity in the ABC subtype of relapsed/refractory de novo diffuse large B-cell lymphoma (DLBCL): Interim results of a multicenter, open-label, phase 2 study. Blood (ASH Annual Meeting Abstracts) 2012, 120, Abstract 686.
86. Younes, A.; Thieblemont, C.; Morschhauser, F.; Flinn, I.; Friedberg, J.W.; Amorim, S.; Hivert, B.; Westin, J.; Vermeulen, J.; Bandyopadhyay, N.; et al. Combination of ibrutinib with rituximab, cyclophosphamide, doxorubicin, vincristine, and prednisone (R-CHOP) for treatment-naive patients with CD20-positive B-cell non-Hodgkin lymphoma: A non-randomised, phase 1b study. Lancet Oncol. 2014, 15, 1019-1026.
87. Maddocks, K.; Christian, B.; Jaglowski, S.; Flynn, J.; Jones, J.A.; Porcu, P.; Wei, L.; Jenkins, C.; Lozanski, G.; Byrd, J.C.; et al. A phase 1/1b study of rituximab, bendamustine, and ibrutinib in patients with untreated and relapsed/refractory non-Hodgkin lymphoma. Blood 2015, 125, 242-248.
88. Dubovsky, J.A.; Beckwith, K.A.; Natarajan, G.; Woyach, J.A.; Jaglowski, S.; Zhong, Y.; Hessler, J.D.; Liu, T.M.; Chang, B.Y.; Larkin, K.M.; et al. Ibrutinib is an irreversible molecular inhibitor of ITK driving a Th1-selective pressure in T lymphocytes. Blood 2013, 122, 2539-2549.
89. Furman, R.R.; Sharman, J.P.; Coutre, S.E.; Cheson, B.D.; Pagel, J.M.; Hillmen, P.; Barrientos, J.C.; Zelenetz, A.D.; Kipps, T.J.; Flinn, I.; et al. Idelalisib and rituximab in relapsed chronic lymphocytic leukemia. N. Engl. J. Med. 2014, 370, 997-1007.
90. Gopal, A.K.; Kahl, B.S.; de Vos, S.; Wagner-Johnston, N.D.; Schuster, S.J.; Jurczak, W.J.; Flinn, I.W.; Flowers, C.R.; Martin, P.; Viardot, A.; et al. PI3Kδ inhibition by idelalisib in patients with relapsed indolent lymphoma. N. Engl. J. Med. 2014, 370, 1008-1018.
91. Kahl, B.S.; Spurgeon, S.E.; Furman, R.R.; Flinn, I.W.; Coutre, S.E.; Brown, J.R.; Benson, D.M.; Byrd, J.C.; Peterman, S.; Cho, Y.; et al. A phase 1 study of the PI3Kδ inhibitor idelalisib in patients with relapsed/refractory mantle cell lymphoma (MCL). Blood 2014, 123, 3398-3405.
92. De Rooij, M.F.; Kuil, A.; Kater, A.P.; Kersten, M.J.; Pals, S.T.; Spaargaren, M. Ibrutinib and idelalisib synergistically target BCR-controlled adhesion in MCL and CLL: A rationale for combination therapy. Blood 2015, 125, 2306-2309.
93. Smith, S.M. New drugs for the treatment of non-Hodgkin lymphomas. Chin. Clin. Oncol. 2015, 4, 14, doi:10.3978/j.issn.2304-3865.2015.03.01.
94. Flinn, I.; Oki, Y.; Patel, M.; Horwitz, S.M.; Foss, F.M.; Sweeney, J.; Allen, K.; Douglas, M.; Steelman, L.; Dunbar, J.; et al. A phase 1 evaluation of duvelisib (IPI-145), a PI3K-δ,γ inhibitor, in patients with relapsed/refractory iNHL. Blood 2014, 124, 802-802.
95. O'Brien, S.; Patel, M.; Kahl, B.S.; Horwitz, S.M.; Foss, F.M.; Porcu, P.; Sweeney, J.; Allen, K.; Faia, K.; Stern, H.M.; et al. Duvelisib (IPI-145), a PI3K-δ,γ inhibitor, is clinically active in patients with relapsed/refractory chronic lymphocytic leukemia. Blood 2014, 124, 3334-3334.
96. Horwitz, S.M.; Porcu, P.; Flinn, I.; Kahl, B.S.; Sweeney, J.; Stern, H.M.; Douglas, M.; Allen, K.; Kelly, P.; Foss, F.M. Duvelisib (IPI-145), a phosphoinositide-3-kinase-δ,γ inhibitor, shows activity in patients with relapsed/refractory T-cell lymphoma. Blood 2014, 124, 803-803.
97. Siddiqi, T.; Rosen, S.T. Novel biologic agents for non-Hodgkin lymphoma and chronic lymphocytic leukemia-part 2: Adoptive cellular immunotherapy, small-molecule inhibitors, and immunomodulation. Oncology (Williston Park, NY) 2015, 29, 299-308.
98. Burris, H.A.; Patel, M.R.; Brander, D.M.; O'Connor, O.A.; Deng, C.; Fenske, T.S.; Gutierrez, M.; Jones, S.; Kuhn, J.; Miskin, H.P.; et al. TGR-1202, a novel once daily PI3Kδ inhibitor, demonstrates clinical activity with a favorable safety profile, lacking hepatotoxicity, in patients with chronic lymphocytic leukemia and B-cell lymphoma. Blood 2014, 124, 1984-1984.
99. Patnaik, A.; Ramanathan, R.K.; Appleman, L.J.; Tolcher, A.W.; Mountz, J.M.; Beerham, M.; Weiss, G.J.; Rasco, D.W.; Lotze, M.T.; Toledo, F.G.; et al. Phase I study of intravenous PI3K inhibitor bay 80-6946: Preliminary activity in patients with relapsed non-Hodgkin lymphoma (NHL) treated in an MTD expansion cohort. Blood (ASH Annual Meeting Abstracts) 2012, 120, Abstract 3704.
100. Morschhauser, F.; Bron, D.; Bouabdallah, K.; Vitolo, U.; Linton, K.; Van Den Neste, E.; Mappa, S.; Giurescu, M.; Childs, B.H.; Zinzani, P.L. Preliminary results of a phase II study of single agent bay 80-6946, a novel PI3K inhibitor, in patients with relapsed/refractory, indolent or aggressive lymphoma. Blood 2013, 122, 87.
101. Carbone, A.; Gloghini, A.; Castagna, L.; Santoro, A.; Carlo-Stella, C. Primary refractory and early-relapsed Hodgkin's lymphoma: Strategies for therapeutic targeting based on the tumour microenvironment. J. Pathol. 2015, 237, 4-13.
102. Phillips, T.J.; Forero-Torres, A.; Sher, T.; Magid Diefenbach, C.S.; Talpaz, M.; Scherle, P.A.; Schaub, R.; Zhou, L.; Pulini, J.; Leopold, L.; et al. Interim analysis of a phase I study of INCB040093, a PI3Kδ inhibitor, alone or in combination with INCB039110, a selective JAK1 inhibitor, in patients (pts) with relapsed or refractory (r/r) B-cell malignancies. J. Clin. Oncol. (ASCO Annual Meeting) 2015, 33, Abstract 8520.
103. Forero-Torres, A.; Barr, P.M.; Magid Diefenbach, C.S.; Sher, T.; Schaub, R.; Zhou, L.; Pulini, J.; Leopold, L.; Spear, M.A.; Talpaz, M.; et al. A phase 1 study of INCB040093, a PI3Kδ inhibitor, alone or in combination with INCB039110, a selective JAK1 inhibitor: Interim results from patients (pts) with relapsed or refractory (r/r) classical Hodgkin lymphoma (cHL). J. Clin. Oncol. (ASCO Meeting Abstracts) 2015, 33, Abstract 8558.
104. Barr, P.M.; Sher, T.; Phillips, T.J.; Lebovic, D.; Zhou, L.; Pulini, J.; Spear, M.A.; Forero-Torres, A. A phase 2 trial of INCB040093 alone or in combination with INCB039110 in patients (pts) with relapsed or refractory (r/r) classical Hodgkin lymphoma (cHL). J. Clin. Oncol. (ASCO Meeting Abstracts) 2015, 33, Abstract TPS8607.
105. Wilson, W.H.; O'Connor, O.A.; Czuczman, M.S.; LaCasce, A.S.; Gerecitano, J.F.; Leonard, J.P.; Tulpule, A.; Dunleavy, K.; Xiong, H.; Chiu, Y.L.; et al. Navitoclax, a targeted high-affinity inhibitor of BCL-2, in lymphoid malignancies: A phase 1 dose-escalation study of safety, pharmacokinetics, pharmacodynamics, and antitumour activity. Lancet Oncol. 2010, 11, 1149-1159.
106. Roberts, A.W.; Advani, R.H.; Kahl, B.S.; Persky, D.; Sweetenham, J.W.; Carney, D.A.; Yang, J.; Busman, T.B.; Enschede, S.H.; Humerickhouse, R.A.; et al. Phase 1 study of the safety, pharmacokinetics, and antitumour activity of the BCL2 inhibitor navitoclax in combination with rituximab in patients with relapsed or refractory CD20 lymphoid malignancies. Br. J. Haematol. 2015, 170, 669-678.
107. Souers, A.J.; Leverson, J.D.; Boghaert, E.R.; Ackler, S.L.; Catron, N.D.; Chen, J.; Dayton, B.D.; Ding, H.; Enschede, S.H.; Fairbrother, W.J.; et al. ABT-199, a potent and selective BCL-2 inhibitor, achieves antitumor activity while sparing platelets. Nat. Med. 2013, 19, 202-208.
108. Davids, M.S.; Seymour John F.; Gerecitano John F.; Kahl, B.S.; Pagel, J.M.; Wierda, W.G.; Anderson, M.A.; Rudersdorf, N.; Gressick, L.A.; Montalvo, N.P.; et al. Phase I study of ABT-199 (GDC-0199) in patients with relapsed/refractory (r/r) non-Hodgkin lymphoma (NHL): responses observed in diffuse large B-cell (DLBCL) and follicular lymphoma (FL) at higher cohort doses. J. Clin. Oncol. (ASCO Annual Meeting) 2014, 32, Abstract 8522.
109. Seymour, J.F.; Davids, M.S.; Pagel, J.M.; Kahl, B.S.; Wierda, W.G.; Puvvada, S.; Gerecitano, J.F.; Kipps, T.J.; Anderson, M.A.; Huang, D.C.; et al. Abt-199 (Gdc-0199) in relapsed/refractory chronic lymphocytic leukemia and small lymphocytic lymphoma: High response rates among patients with high risk disease features including unmutated ighv. Haemotologica. (19th Congress of the European Hematology Association) 2014, 99, Abstract S702.
110. Friedberg, J.W.; Mahadevan, D.; Cebula, E.; Persky, D.; Lossos, I.; Agarwal, A.B.; Jung, J.; Burack, R.; Zhou, X.; Leonard, E.J.; et al. Phase II study of alisertib, a selective aurora a kinase inhibitor, in relapsed and refractory aggressive B-and T-cell non-Hodgkin lymphomas. J. Clin. Oncol. 2014, 32, 44-50.
111. Barr, P.M.; Li, H.; Spier, C.; Mahadevan, D.; LeBlanc, M.; Ul Haq, M.; Huber, B.D.; Flowers, C.R.; Wagner-Johnston, N.D.; Horwitz, S.M.; et al. Phase II intergroup trial of alisertib in relapsed and refractory peripheral T-Cell lymphoma and transformed mycosis fungoides: SWOG 1108. J. Clin. Oncol. 2015, 33, 2399-2404.
112. Mahadevan, D.; Morales, C.; Cooke, L.S.; Manziello, A.; Mount, D.W.; Persky, D.O.; Fisher, R.I.; Miller, T.P.; Qi, W. Alisertib added to rituximab and vincristine is synthetic lethal and potentially curative in mice with aggressive DLBCL co-overexpressing MYC and BCL2. PLoS ONE 2014, 9, e95184.