Case Report of a Fatal Serious Adverse Event Upon Administration of T Cells Transduced with a MART-1-specific T-cell Receptor

Molecular Therapy

Volumn 23, Issue 9, 2015, Pages 1541-1550

  Van Den Berg, Joost H ^a,b   Gomez Eerland, Raquel ^a   Van De Wiel, Bart ^a   Hulshoff, Lenie ^c   Van Den Broek, Daan ^c   Bins, Adriaan ^c   Tan, Hanno L ^d   Harper, Jane V ^e   Hassan, Namir J ^e   Jakobsen, Bent K ^e   Jorritsma, Annelies ^a   Blank, Christian U ^a,c   Schumacher, Ton N M ^a   Haanen, John B A G ^a,c  

^a Department of Radiation Oncology   (United States)

^b Amsterdam Biotherapeutics Unit (AmBTU)   (Netherlands)

^c NETHERLANDS CANCER INSTITUTE   (Netherlands)

^d UNIVERSITY OF AMSTERDAM   (Netherlands)

^e Immunocore Limited   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMOXICILLIN; C REACTIVE PROTEIN; CD27 ANTIGEN; CD3 ANTIGEN; CD4 ANTIGEN; CD45RA ANTIGEN; CD8 ANTIGEN; CHEMOKINE RECEPTOR CCR7; CYCLOPHOSPHAMIDE; EPITOPE; FLUDARABINE; GAMMA INTERFERON; GRANZYME B; HLA A ANTIGEN; IMIPENEM; INTERLEUKIN 2; INTERLEUKIN 6; IPILIMUMAB; L SELECTIN; MELAN A; MEROPENEM; MITOGEN ACTIVATED PROTEIN KINASE KINASE INHIBITOR; NORADRENALIN; OXYGEN; PROCALCITONIN; PROGRAMMED DEATH 1 RECEPTOR; T LYMPHOCYTE RECEPTOR; VANCOMYCIN; VORICONAZOLE; LYMPHOCYTE ANTIGEN RECEPTOR;

ADULT; ANTIGEN EXPRESSION; ANTIGEN RECOGNITION; APHERESIS; ARTICLE; ARTIFICIAL VENTILATION; ASCITES; AUTOPSY; BLOOD SAMPLING; BRAIN DAMAGE; BRAIN HEMORRHAGE; BRAIN METASTASIS; CASE REPORT; CELL CULTURE; CELL ISOLATION; CROSS REACTION; CYANOSIS; CYTOKINE RELEASE SYNDROME; DEATH; DRUG SUBSTITUTION; DRUG WITHDRAWAL; EDEMA; EPILEPSY; EXTENDED SPECTRUM BETA LACTAMASE PRODUCING ESCHERICHIA COLI; FECES CULTURE; FEMALE; FEVER; GENETIC TRANSDUCTION; HEART ARREST; HEART FAILURE; HEART MUSCLE CELL; HUMAN; INDUCED HYPOTHERMIA; INFLAMMATION; LOW DRUG DOSE; LUNG LAVAGE; LUNG METASTASIS; LYMPH NODE METASTASIS; LYMPHOCYTE TRANSFER; METASTATIC MELANOMA; MULTIPLE ORGAN FAILURE; PARACENTESIS; PELVIS CANCER; RESUSCITATION; RETROPERITONEAL CANCER; SEPSIS; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; ADOPTIVE IMMUNOTHERAPY; ADVERSE EFFECTS; BIOLOGICAL THERAPY; CANCER STAGING; FATALITY; GENETICS; IMMUNOLOGY; MELANOMA; METABOLISM; PROCEDURES; TUMOR ASSOCIATED LEUKOCYTE;

ADULT; CELL- AND TISSUE-BASED THERAPY; FATAL OUTCOME; FEMALE; HUMANS; IMMUNOTHERAPY, ADOPTIVE; LYMPHOCYTES, TUMOR-INFILTRATING; MART-1 ANTIGEN; MELANOMA; NEOPLASM STAGING; RECEPTORS, ANTIGEN, T-CELL; T-CELL ANTIGEN RECEPTOR SPECIFICITY; T-LYMPHOCYTES; TRANSDUCTION, GENETIC;

EID: 84940720703     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2015.60     Document Type: Article

References (39)

1. Rosenberg, SA, Yang, JC, Sherry, RM, Kammula, US, Hughes, MS, Phan, GQ et al. (2011). Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy. Clin Cancer Res 17: 4550-4557.
2. Morgan, RA, Dudley, ME, Wunderlich, JR, Hughes, MS, Yang, JC, Sherry, RM et al. (2006). Cancer regression in patients after transfer of genetically engineered lymphocytes. Science 314: 126-129.
3. Johnson, LA, Morgan, RA, Dudley, ME, Cassard, L, Yang, JC, Hughes, MS et al. (2009). Gene therapy with human and mouse T-cell receptors mediates cancer regression and targets normal tissues expressing cognate antigen. Blood 114: 535-546.
4. Robbins, PF, Morgan, RA, Feldman, SA, Yang, JC, Sherry, RM, Dudley, ME et al. (2011). Tumor regression in patients with metastatic synovial cell sarcoma and melanoma using genetically engineered lymphocytes reactive with NY-ESO-1. J Clin Oncol 29: 917-924.
5. Chodon, T, Comin-Anduix, B, Chmielowski, B, Koya, RC, Wu, Z, Auerbach, M et al. (2014). Adoptive transfer of MART-1 T-cell receptor transgenic lymphocytes and dendritic cell vaccination in patients with metastatic melanoma. Clin Cancer Res 20: 2457-2465.
6. Parkhurst, MR, Yang, JC, Langan, RC, Dudley, ME, Nathan, DA, Feldman, SA et al. (2011). T cells targeting carcinoembryonic antigen can mediate regression of metastatic colorectal cancer but induce severe transient colitis. Mol Ther 19: 620-626.
7. Morgan, RA, Chinnasamy, N, Abate-Daga, D, Gros, A, Robbins, PF, Zheng, Z et al. (2013). Cancer regression and neurological toxicity following anti-MAGE-A3 TCR gene therapy. J Immunother 36: 133-151.
8. Bendle, GM, Linnemann, C, Hooijkaas, AI, Bies, L, de Witte, MA, Jorritsma, A et al. (2010). Lethal graft-versus-host disease in mouse models of T cell receptor gene therapy. Nat Med 16: 565-70, 1p following 570.
9. Cameron, BJ, Gerry, AB, Dukes, J, Harper, JV, Kannan, V, Bianchi, FC et al. (2013). Identification of a Titin-derived HLA-A1-presented peptide as a cross-reactive target for engineered MAGE A3-directed T cells. Sci Transl Med 5: 197ra103.
10. Linette, GP, Stadtmauer, EA, Maus, MV, Rapoport, AP, Levine, BL, Emery, L et al. (2013). Cardiovascular toxicity and titin cross-reactivity of affinity-enhanced T cells in myeloma and melanoma. Blood 122: 863-871.
11. Porter, DL, Levine, BL, Kalos, M, Bagg, A and June, CH (2011). Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N Engl J Med 365: 725-733.
12. Kalos, M, Levine, BL, Porter, DL, Katz, S, Grupp, SA, Bagg, A et al. (2011). T cells with chimeric antigen receptors have potent antitumor effects and can establish memory in patients with advanced leukemia. Sci Transl Med. 3: 95ra73.
13. Kochenderfer, JN, Dudley, ME, Feldman, SA, Wilson, WH, Spaner, DE, Maric, I et al. (2012). 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 119: 2709-2720.
14. Grupp, SA, Kalos, M, Barrett, D, Aplenc, R, Porter, DL, Rheingold, SR et al. (2013). Chimeric antigen receptor-modified T cells for acute lymphoid leukemia. N Engl J Med 368: 1509-1518.
15. Davila, ML, Riviere, I, Wang, X, Bartido, S, Park, J, Curran, K et al. (2014). Efficacy and toxicity management of 19-28z CAR T cell therapy in B cell acute lymphoblastic leukemia. Sci Transl Med 6: 224ra25.
16. Valmori, D, Dutoit, V, Schnuriger, V, Quiquerez, AL, Pittet, MJ, Guillaume, P et al. (2002). Vaccination with a Melan-A peptide selects an oligoclonal T cell population with increased functional avidity and tumor reactivity. J Immunol 168: 4231-4240.
17. Dietrich, PY, Le Gal, FA, Dutoit, V, Pittet, MJ, Trautman, L, Zippelius, A et al. (2003). Prevalent role of TCR alpha-chain in the selection of the preimmune repertoire specific for a human tumor-associated self-antigen. J Immunol 170: 5103-5109.
18. Jorritsma, A, Gomez-Eerland, R, Dokter, M, van de Kasteele, W, Zoet, YM, Doxiadis, II et al. (2007). Selecting highly affine and well-expressed TCRs for gene therapy of melanoma. Blood 110: 3564-3572.
19. Cohen, CJ, Zhao, Y, Zheng, Z, Rosenberg, SA and Morgan, RA (2006). Enhanced antitumor activity of murine-human hybrid T-cell receptor (TCR) in human lymphocytes is associated with improved pairing and TCR/CD3 stability. Cancer Res 66: 8878-8886.
20. Kuball, J, Dossett, ML, Wolfl, M, Ho, WY, Voss, RH, Fowler, C et al. (2007). Facilitating matched pairing and expression of TCR chains introduced into human T cells. Blood 109: 2331-2338.
21. Cohen, CJ, Li, YF, El-Gamil, M, Robbins, PF, Rosenberg, SA and Morgan, RA (2007). Enhanced antitumor activity of T cells engineered to express T-cell receptors with a second disulfide bond. Cancer Res 67: 3898-3903.
22. Szymczak, AL, Workman, CJ, Wang, Y, Vignali, KM, Dilioglou, S, Vanin, EF et al. (2004). Correction of multi-gene deficiency in vivo using a single 'self-cleaving' 2A peptide-based retroviral vector. Nat Biotechnol 22: 589-594.
23. Kaneko, S, Mastaglio, S, Bondanza, A, Ponzoni, M, Sanvito, F, Aldrighetti, L et al. (2009). IL-7 and IL-15 allow the generation of suicide gene-modified alloreactive self-renewing central memory human T lymphocytes. Blood 113: 1006-1015.
24. Kaiser, AD, Gadiot, J, Guislain, A and Blank, CU (2013). Mimicking homeostatic proliferation in vitro generates T cells with high anti-tumor function in nonlymphopenic hosts. Cancer Immunol Immunother 62: 503-515.
25. Gomez-Eerland, R, Nuijen, B, Heemskerk, B, van Rooij, N, van den Berg, JH, Beijnen, JH et al. (2014). Manufacture of gene-modified human T-cells with a memory stem/central memory phenotype. Hum Gene Ther Methods 25: 277-287.
26. Brentjens, R, Yeh, R, Bernal, Y, Riviere, I and Sadelain, M (2010). Treatment of chronic lymphocytic leukemia with genetically targeted autologous T cells: case report of an unforeseen adverse event in a phase I clinical trial. Mol Ther 18: 666-668.
27. Smeding, L, Plötz, FB, Groeneveld, AB and Kneyber, MC (2012). Structural changes of the heart during severe sepsis or septic shock. Shock 37: 449-456.
28. Patil, VK, Morjaria, JB, De Villers, F and Babu, SK (2012). Associations between procalcitonin and markers of bacterial sepsis. Medicina (Kaunas) 48: 383-387.
29. Morandi, P, Ruffini, PA, Benvenuto, GM, Raimondi, R and Fosser, V (2005). Cardiac toxicity of high-dose chemotherapy. Bone Marrow Transplant 35: 323-334.
30. de Jonge, ME, Huitema, AD, Rodenhuis, S and Beijnen, JH (2005). Clinical pharmacokinetics of cyclophosphamide. Clin Pharmacokinet 44: 1135-1164.
31. Rosenberg, SA and Dudley, ME (2009). Adoptive cell therapy for the treatment of patients with metastatic melanoma. Curr Opin Immunol 21: 233-240.
32. López, L, Arai, K, Giménez, E, Jiménez, M, Pascuzo, C, Rodríguez-Bonfante, C et al. (2006). [C-reactive protein and interleukin-6 serum levels increase as Chagas disease progresses towards cardiac failure]. Rev Esp Cardiol 59: 50-56.
33. Varpula, M, Pulkki, K, Karlsson, S, Ruokonen, E and Pettilä, V; FINNSEPSIS Study Group (2007). Predictive value of N-terminal pro-brain natriuretic peptide in severe sepsis and septic shock. Crit Care Med 35: 1277-1283.
34. De Herdt, V, Dumont, F, Hénon, H, Derambure, P, Vonck, K, Leys, D et al. (2011). Early seizures in intracerebral hemorrhage: incidence, associated factors, and outcome. Neurology 77: 1794-1800.
35. McLean, BN and Wimalaratna, S (2007). Sudden death in epilepsy recorded in ambulatory EEG. J Neurol Neurosurg Psychiatr 78: 1395-1397.
36. Rosenberg, SA (2010). Of mice, not men: No evidence for graft-versus-host disease in humans receiving T-cell receptor-transduced autologous T cells. Mol Ther 18: 1744-1745.
37. Morgan, RA, Yang, JC, Kitano, M, Dudley, ME, Laurencot, CM and Rosenberg, SA (2010). Case report of a serious adverse event following the administration of T cells transduced with a chimeric antigen receptor recognizing ERBB2. Mol Ther 18: 843-851.
38. Weber, J, Yang, JC, Topalian, SL, Parkinson, DR, Schwartzentruber, DS, Ettinghausen, SE et al. (1993). Phase I trial of subcutaneous interleukin-6 in patients with advanced malignancies. J Clin Oncol 11: 499-506.
39. Toebes, M, Coccoris, M, Bins, A, Rodenko, B, Gomez, R, Nieuwkoop, NJ et al. (2006). Design and use of conditional MHC class I ligands. Nat Med 12: 246-251.