Immunotherapy: Opportunities, risks and future perspectives

Cytotherapy

Volumn 16, Issue 4, 2014, Pages S120-S129

  Hildebrandt, Martin ^a   Peggs, Karl ^b   Uharek, Lutz ^c   Bollard, Catherine M ^d   Heslop, Helen E ^e  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY COLLEGE HOSPITAL   (United Kingdom)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^d CHILDREN'S NATIONAL MEDICAL CENTER   (United States)

^e BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Clinical trials; Gene therapy; Immunotherapy; Safety; T cell receptor; Treatment efficacy

Indexed keywords

LEUKEMIA ANTIGEN; LYMPHOMA ASSOCIATED ANTIGEN; T LYMPHOCYTE RECEPTOR; TUMOR ANTIGEN; UNCLASSIFIED DRUG; VIRUS ANTIGEN; CANCER VACCINE; LYMPHOCYTE ANTIGEN RECEPTOR;

ADOPTIVE TRANSFER; ADVERSE OUTCOME; BIOTECHNOLOGY; CANCER IMMUNOTHERAPY; CELL BASED GENE THERAPY; CELL SPECIFICITY; CELL THERAPY; CLINICAL EFFECTIVENESS; CLINICAL RESEARCH; DRUG INDUSTRY; GENE TRANSFER; GENETIC ENGINEERING; GENETIC TRANSDUCTION; HEMATOLOGIC MALIGNANCY; HOST PATHOGEN INTERACTION; HUMAN; IMMUNOSTIMULATION; LYMPHOCYTE TRANSFER; NATURAL KILLER CELL; NONHUMAN; PRACTICE GUIDELINE; PRIORITY JOURNAL; PROTEIN TARGETING; REVIEW; RISK BENEFIT ANALYSIS; RISK MANAGEMENT; RISK REDUCTION; T LYMPHOCYTE; BIOLOGICAL THERAPY; CLINICAL TRIAL (TOPIC); GENE THERAPY; GENETICS; IMMUNOLOGY; IMMUNOTHERAPY; SAFETY; SPECIES DIFFERENCE; THERAPY;

CLINICAL TRIALS; GENE THERAPY; IMMUNOTHERAPY; SAFETY; T CELL RECEPTOR; TREATMENT EFFICACY;

CANCER VACCINES; CELL- AND TISSUE-BASED THERAPY; CLINICAL TRIALS AS TOPIC; GENETIC THERAPY; HUMANS; IMMUNOTHERAPY; RECEPTORS, ANTIGEN, T-CELL; SPECIES SPECIFICITY;

EID: 84907981233     PISSN: 14653249     EISSN: 14772566     Source Type: Journal    
DOI: 10.1016/j.jcyt.2014.02.001     Document Type: Review

References (68)

1. Kalos M., Levine B.L., Porter D.L., Katz S., Grupp S.A., Bagg A., et al. Tcells with chimeric antigen receptors have potent antitumor effects and can establish memory in patients with advanced leukemia. Sci Transl Med 2011, 3:95ra73.
2. Brentjens R.J., Davila M.L., Riviere I., Park J., Wang X., Cowell L.G., et al. CD19-targeted T cells rapidly induce molecular remissions in adults with chemotherapy-refractory acute lymphoblastic leukemia. Sci Transl Med 2013, 5:177ra38.
3. Bollard CM, Gottschalk S, Torrano V, Diouf O, Ku S, Hazrat Y, et al. Sustained complete responses in lymphoma patients receiving autologous cytotoxic T lymphocytes targeting Epstein-Barr virus latent membrane protein [published online ahead of print December 16, 2013]. J Clin Oncol.
4. Kochenderfer J.N., Dudley M.E., Feldman S.A., Wilson W.H., Spaner D.E., 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 Tcells. Blood 2012, 119:2709-2720.
5. Rosenberg S.A., Yang J.C., Sherry R.M., Kammula U.S., Hughes M.S., Phan G.Q., et al. Durable complete responses in heavily pretreated patients with metastatic melanoma using Tcell transfer immunotherapy. Clin Cancer Res 2011, 17:4550-4557.
6. Peggs K.S., Thomson K., Samuel E., Dyer G., Armoogum J., Chakraverty R., et al. Directly selected cytomegalovirus-reactive donor T cells confer rapid and safe systemic reconstitution of virus-specific immunity following stem cell transplantation. Clin Infect Dis 2011, 52:49-57.
7. Bollard C.M., Rooney C.M., Heslop H.E. T-cell therapy in the treatment of post-transplant lymphoproliferative disease. Nat Rev Clin Oncol 2012, 9:510-519.
8. Chapuis A.G., Ragnarsson G.B., Nguyen H.N., Chaney C.N., Pufnock J.S., Schmitt T.M., et al. Transferred WT1-reactive CD8+ T cells can mediate antileukemic activity and persist in post-transplant patients. Sci Transl Med 2013, 5:174ra27.
9. Grupp S.A., Kalos M., Barrett D., Aplenc R., Porter D.L., Rheingold S.R., et al. Chimeric antigen receptor-modified T cells for acute lymphoid leukemia. NEngl J Med 2013, 368:1509-1518.
10. Heslop H.E., Slobod K.S., Pule M.A., Hale G.A., Rousseau A., Smith C.A., et al. Long-term outcome of EBV-specific T-cell infusions to prevent or treat EBV-related lymphoproliferative disease in transplant recipients. Blood 2010, 115:925-935.
11. Scholler J., Brady T.L., Binder-Scholl G., Hwang W.T., Plesa G., Hege K.M., et al. Decade-long safety and function of retroviral-modified chimeric antigen receptor T cells. Sci Transl Med 2012, 4:132-153.
12. Linette G.P., Stadtmauer E.A., Maus M.V., Rapoport A.P., Levine B.L., Emery L., et al. Cardiovascular toxicity and titin cross-reactivity of affinity enhanced T cells in myeloma and melanoma. Blood 2013, 122:863-871.
13. Morgan R.A., Yang J.C., Kitano M., Dudley M.E., Laurencot C.M., Rosenberg S.A. Case report of a serious adverse event following the administration of T cells transduced with a chimeric antigen receptor recognizing ERBB2. Mol Ther 2010, 18:843-851.
14. Suntharalingam G., Perry M.R., Ward S., Brett S.J., Castello-Cortes A., Brunner M.D., et al. Cytokine storm in a phase 1 trial of the anti-CD28 monoclonal antibody TGN1412. NEngl J Med 2006, 355:1018-1028.
15. Expert Scientific Group on phase one clinical trials. 11-30-2006. ISBN-10 0 11 703722 2.
16. Heslop H.E., Ng C.Y., Li C., Smith C.A., Loftin S.K., Krance R.A., et al. Long-term restoration of immunity against Epstein-Barr virus infection by adoptive transfer of gene-modified virus-specific T lymphocytes. Nat Med 1996, 2:551-555.
17. Riddell S.R., Watanabe K.S., Goodrich J.M., Li C.R., Agha M.E., Greenberg P.D. Restoration of viral immunity in immunodeficient humans by the adoptive transfer of T cell clones. Science 1992, 257:238-241.
18. Leen A.M., Myers G.D., Sili U., Huls M.H., Weiss H., Leung K.S., et al. Monoculture-derived T lymphocytes specific for multiple viruses expand and produce clinically relevant effects in immunocompromised individuals. Nat Med 2006, 12:1160-1166.
19. Peggs K.S., Verfuerth S., Pizzey A., Khan N., Guiver M., Moss P.A., et al. Adoptive cellular therapy for early cytomegalovirus infection after allogeneic stem-cell transplantation with virus-specific T-cell lines. Lancet 2003, 362:1375-1377.
20. Peggs K.S., Verfuerth S., Pizzey A., Chow S.L., Thomson K., Mackinnon S. Cytomegalovirus-specific T cell immunotherapy promotes restoration of durable functional antiviral immunity following allogeneic stem cell transplantation. Clin Infect Dis 2009, 49:1851-1860.
21. Einsele H., Roosnek E., Rufer N., Sinzger C., Riegler S., Loffler J., et al. Infusion of cytomegalovirus (CMV)-specific T cells for the treatment of CMV infection not responding to antiviral chemotherapy. Blood 2002, 99:3916-3922.
22. Trivedi D., Williams R.Y., O'Reilly R.J., Koehne G. Generation of CMV-specific T lymphocytes using protein-spanning pools of pp65-derived overlapping pentadecapeptides for adoptive immunotherapy. Blood 2005, 105:2793-2801.
23. Blyth E., Clancy L., Simms R., Ma C.K., Burgess J., Deo S., et al. Donor-derived CMV-specific T cells reduce the requirement for CMV-directed pharmacotherapy after allogeneic stem cell transplantation. Blood 2013, 121:3745-3758.
24. Gerdemann U., Katari U.L., Papadopoulou A., Keirnan J.M., Craddock J.A., Liu H., et al. Safety and clinical efficacy of rapidly-generated trivirus-directed T cells as treatment for adenovirus, EBV, and CMV infections after allogeneic hematopoietic stem cell transplant. Mol Ther 2013, 21:2113-2121.
25. Feuchtinger T., Matthes-Martin S., Richard C., Lion T., Fuhrer M., Hamprecht K., et al. Safe adoptive transfer of virus-specific T-cell immunity for the treatment of systemic adenovirus infection after allogeneic stem cell transplantation. Br J Haematol 2006, 134:64-76.
26. Feuchtinger T., Opherk K., Bethge W.A., Topp M.S., Schuster F.R., Weissinger E.M., et al. Adoptive transfer of pp65-specific T cells for the treatment of chemorefractory cytomegalovirus disease or reactivation after haploidentical and matched unrelated stem cell transplantation. Blood 2010, 116:4360-4367.
27. Icheva V., Kayser S., Wolff D., Tuve S., Kyzirakos C., Bethge W., et al. Adoptive transfer of Epstein-Barr virus (EBV) nuclear antigen 1-specific T cells as treatment for EBV reactivation and lymphoproliferative disorders after allogeneic stem-cell transplantation. JClin Oncol 2013, 31:39-48.
28. Cobbold M., Khan N., Pourgheysari B., Tauro S., McDonald D., Osman H., et al. Adoptive transfer of cytomegalovirus-specific CTL to stem cell transplant patients after selection by HLA-peptide tetramers. JExp Med 2005, 202:379-386.
29. Schmitt A., Tonn T., Busch D.H., Grigoleit G.U., Einsele H., Odendahl M., et al. Adoptive transfer and selective reconstitution of streptamer-selected cytomegalovirus-specific CD8+ T cells leads to virus clearance in patients after allogeneic peripheral blood stem cell transplantation. Transfusion 2011, 51:591-599.
30. Uhlin M., Gertow J., Uzunel M., Okas M., Berglund S., Watz E., et al. Rapid salvage treatment with virus-specific T cells for therapy-resistant disease. Clin Infect Dis 2012, 55:1064-1073.
31. Melenhorst J.J., Leen A.M., Bollard C.M., Quigley M.F., Price D.A., Rooney C.M., et al. Allogeneic virus-specific T cells with HLA alloreactivity do not produce GVHD in human subjects. Blood 2010, 116:4700-4702.
32. Haque T., Wilkie G.M., Jones M.M., Higgins C.D., 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, 110:1123-1131.
33. Leen A.M., Bollard C.M., Mendizabal A.M., Shpall E.J., Szabolcs P., Antin J.H., et al. Multicenter study of banked third-party virus-specific T cells to treat severe viral infections after hematopoietic stem cell transplantation. Blood 2013, 121:5113-5123.
34. Hanley P.J., Cruz C.R., Savoldo B., Leen A.M., Stanojevic M., Khalil M., et al. Functionally active virus-specific T cells that target CMV, adenovirus, and EBV can be expanded from naive T-cell populations in cord blood and will target a range of viral epitopes. Blood 2009, 114:1958-1967.
35. Gerdemann U., Keirnan J.M., Katari U.L., Yanagisawa R., Christin A.S., Huye L.E., et al. Rapidly generated multivirus-specific cytotoxic T lymphocytes for the prophylaxis and treatment of viral infections. Mol Ther 2012, 20:1622-1632.
36. Teschner D., Distler E., Wehler D., Frey M., Marandiuc D., Langeveld K., et al. Depletion of naive T cells using clinical grade magnetic CD45RA beads: a new approach for GVHD prophylaxis. Bone Marrow Transplant 2014, 49:138-144.
37. Nicholson E., Ghorashian S., Stauss H. Improving TCR gene therapy for treatment of haematological malignancies. Adv Hematol 2012, 2012:404081.
38. Davila M.L., Brentjens R., Wang X., Riviere I., Sadelain M. How do CARs work? Early insights from recent clinical studies targeting CD19. Oncoimmunology 2012, 1:1577-1583.
39. Clay T.M., Custer M.C., Sachs J., Hwu P., Rosenberg S.A., Nishimura M.I. Efficient transfer of a tumor antigen-reactive TCR to human peripheral blood lymphocytes confers anti-tumor reactivity. JImmunol 1999, 163:507-513.
40. Schroten C., Kraaij R., Veldhoven J.L., Berrevoets C.A., den Bakker M.A., Ma Q., et al. Tcell activation upon exposure to patient-derived tumor tissue: a functional assay to select patients for adoptive T cell therapy. JImmunol Methods 2010, 359:11-20.
41. Singh H., Manuri P.R., Olivares S., Dara N., Dawson M.J., Huls H., et al. Redirecting specificity of T-cell populations for CD19 using the Sleeping Beauty system. Cancer Res 2008, 68:2961-2971.
42. Gattinoni L., Lugli E., Ji Y., Pos Z., Paulos C.M., Quigley M.F., et al. Ahuman memory T cell subset with stem cell-like properties. Nat Med 2011, 17:1290-1297.
43. Dudley M.E., Yang J.C., Sherry R., Hughes M.S., Royal R., Kammula U., et al. Adoptive cell therapy for patients with metastatic melanoma: evaluation of intensive myeloablative chemoradiation preparative regimens. JClin Oncol 2008, 26:5233-5239.
44. Ciceri F., Bonini C., Stanghellini M.T., Bondanza A., Traversari C., Salomoni M., et al. Infusion of suicide-gene-engineered donor lymphocytes after family haploidentical haemopoietic stem-cell transplantation for leukaemia (the TK007 trial): a non-randomised phase I-II study. Lancet Oncol 2009, 10:489-500.
45. Di Stasi A., Tey S.K., Dotti G., Fujita Y., Kennedy-Nasser A., Martinez C., et al. Inducible apoptosis as a safety switch for adoptive cell therapy. NEngl J Med 2011, 365:1673-1683.
46. Introna M., Barbui A.M., Bambacioni F., Casati C., Gaipa G., Borleri G., et al. Genetic modification of human T cells with CD20: a strategy to purify and lyse transduced cells with anti-CD20 antibodies. Hum Gene Ther 2000, 11:611-620.
47. Maus M.V., Beatty A.R., Albelda S.M., Levine B., Liu X., Zhao Y., et al. Tcells expressing chimeric antigen receptors can cause anaphylaxis in humans. Cancer Immunol Res 2013, 1:26-31.
48. Newrzela S., Cornils K., Li Z., Baum C., Brugman M.H., Hartmann M., et al. Resistance of mature T cells to oncogene transformation. Blood 2008, 112:2278-2286.
49. Cameron B.J., Gerry A.B., Dukes J., Harper J.V., Kannan V., Bianchi F.C., et al. Identification of a Titin-derived HLA-A1-presented peptide as a cross-reactive target for engineered MAGE A3-directed T cells. Sci Transl Med 2013, 5:197ra103.
50. Morgan R.A., Chinnasamy N., Abate-Daga D., Gros A., Robbins P.F., Zheng Z., et al. Cancer regression and neurological toxicity following anti-MAGE-A3 TCR gene therapy. JImmunother 2013, 36:133-151.
51. Brentjens R.J., Riviere I., Park J.H., Davila M.L., Wang X., Stefanski J., et al. Safety and persistence of adoptively transferred autologous CD19-targeted T cells in patients with relapsed or chemotherapy refractory B-cell leukemias. Blood 2011, 118:4817-4828.
52. Savoldo B., Ramos C.A., Liu E., Mims M.P., Keating M.J., Carrum G., et al. CD28 costimulation improves expansion and persistence of chimeric antigen receptor-modified T cells in lymphoma patients. JClin Invest 2011, 121:1822-1826.
53. Kershaw M.H., Westwood J.A., Parker L.L., Wang G., Eshhar Z., Mavroukakis S.A., et al. Aphase I study on adoptive immunotherapy using gene-modified T cells for ovarian cancer. Clin Cancer Res 2006, 12(20 Pt 1):6106-6115.
54. Louis C.U., Savoldo B., Dotti G., Pule M., Yvon E., Myers G.D., et al. Antitumor activity and long-term fate of chimeric antigen receptor-positive T cells in patients with neuroblastoma. Blood 2011, 118:6050-6056.
55. Rezvani K., Grube M., Brenchley J.M., Sconocchia G., Fujiwara H., Price D.A., et al. Functional leukemia-associated antigen-specific memory CD8+ T cells exist in healthy individuals and in patients with chronic myelogenous leukemia before and after stem cell transplantation. Blood 2003, 102:2892-2900.
56. Cruz C.R., Micklethwaite K.P., Savoldo B., Ramos C.A., 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, 122:2965-2973.
57. Cohen J.I. Benign and malignant Epstein-Barr virus-associated B-cell lymphoproliferative diseases. Semin Hematol 2003, 40:116-123.
58. Young L.S., Murray P.G. Epstein-Barr virus and oncogenesis: from latent genes to tumours. Oncogene 2003, 22:5108-5121.
59. Bollard C.M., Aguilar L., Straathof K.C., Gahn B., Huls M.H., Rousseau A., et al. Cytotoxic T lymphocyte therapy for Epstein-Barr virus+ Hodgkin's disease. JExp Med 2004, 200:1623-1633.
60. Bollard C.M., Rossig C., Calonge M.J., Huls M.H., Wagner H.J., Massague J., et al. Adapting a transforming growth factor beta-related tumor protection strategy to enhance antitumor immunity. Blood 2002, 99:3179-3187.
61. Bollard C.M., Gottschalk S., Leen A.M., Weiss H., Straathof K.C., Carrum G., et al. Complete responses of relapsed lymphoma following genetic modification of tumor-antigen presenting cells and T-lymphocyte transfer. Blood 2007, 110:2838-2845.
62. Dao T., Scheinberg D.A. Peptide vaccines for myeloid leukaemias. Best Pract Res Clin Haematol 2008, 21:391-404.
63. Quintarelli C., Dotti G., Hasan S.T., De A.B., Hoyos V., Errichiello S., et al. High-avidity cytotoxic T lymphocytes specific for a new PRAME-derived peptide can target leukemic and leukemic-precursor cells. Blood 2011, 117:3353-3362.
64. Weber G., Caruana I., Rouce R.H., Barrett A.J., Gerdemann U., Leen A.M., et al. Generation of tumor antigen-specific T cell lines from pediatric patients with acute lymphoblastic leukemia: implications for immunotherapy. Clin Cancer Res 2013, 19:5079-5091.
65. Weber G., Gerdemann U., Caruana I., Savoldo B., Hensel N.F., Rabin K.R., et al. Generation of multi-leukemia antigen-specific T cells to enhance the graft-versus-leukemia effect after allogeneic stem cell transplant. Leukemia 2013, 27:1538-1547.
66. Gerdemann U., Katari U., Christin A.S., Cruz C.R., Tripic T., Rousseau A., et al. Cytotoxic T lymphocytes simultaneously targeting multiple tumor-associated antigens to treat EBV negative lymphoma. Mol Ther 2011, 19:2258-2268.
67. Shafer J.A., Cruz C.R., Leen A.M., Ku S., Lu A., Rousseau A., et al. Antigen-specific cytotoxic T lymphocytes can target chemoresistant side-population tumor cells in Hodgkin lymphoma. Leuk Lymphoma 2010, 51:870-880.
68. Cruz C.R., Gerdemann U., Leen A.M., Shafer J.A., Ku S., Tzou B., et al. Improving T-cell therapy for relapsed EBV-negative Hodgkin lymphoma by targeting upregulated MAGE-A4. Clin Cancer Res 2011, 17:7058-7066.