Chimeric antigen receptor T cell–mediated neurotoxicity in nonhuman primates

Cancer Discovery

Volumn 8, Issue 6, 2018, Pages 750-763

  Taraseviciute, Agne ^a,b,c   Tkachev, Victor ^a,b,c   Ponce, Rafael ^d   Turtle, Cameron J ^b   Snyder, Jessica M ^e   Liggitt, H Denny ^e   Myerson, David ^b,e   Gonzalez Cuyar, Luis ^e   Baldessari, Audrey ^e   English, Chris ^e   Yu, Alison ^a   Zheng, Hengqi ^a,c   Furlan, Scott N ^a,b,c   Hunt, Daniel J ^a   Hoglund, Virginia ^a   Finney, Olivia ^a   Brakke, Hannah ^a   Blazar, Bruce R ^f   Berger, Carolina ^b   Riddell, Stanley R ^b   Gardner, Rebecca ^a   Kean, Leslie S ^a,b,c   Jensen, Michael C ^a,b,c   more..

^a SEATTLE CHILDREN S RESEARCH INSTITUTE   (United States)

^b Fred Hutchinson Cancer Research Center   (United States)

^c UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^d Juno Therapeutics   (United States)

^e UNIVERSITY OF WASHINGTON   (United States)

^f UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD20 ANTIGEN; CYCLOPHOSPHAMIDE; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 6; INTERLEUKIN 8; VASCULOTROPIN; LYMPHOCYTE ANTIGEN RECEPTOR;

ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ANIMAL MODEL; APLASIA; ARTICLE; B LYMPHOCYTE; CELL EXPANSION; CEREBROSPINAL FLUID LEVEL; CHIMERIC ANTIGEN RECEPTOR IMMUNOTHERAPY; CHRONIC MYELOID LEUKEMIA CELL LINE; CYTOTOXIC T LYMPHOCYTE; EX VIVO STUDY; HEMATOLOGIC MALIGNANCY; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HUMAN IMMUNODEFICIENCY VIRUS; IMMUNOPHENOTYPING; IN VIVO STUDY; LENTIVIRUS INFECTION; NEUROTOXICITY; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIMATE; RHESUS MONKEY; SIMIAN IMMUNODEFICIENCY VIRUS; ADOPTIVE IMMUNOTHERAPY; ANIMAL; AUTOTRANSPLANTATION; DISEASE MODEL; IMMUNOLOGY; K-562 CELL LINE; TOXICITY AND INTOXICATION; TUMOR CELL LINE;

ANIMALS; ANTIGENS, CD20; CELL LINE, TUMOR; CYCLOPHOSPHAMIDE; DISEASE MODELS, ANIMAL; HUMANS; IMMUNOTHERAPY, ADOPTIVE; K562 CELLS; MACACA MULATTA; NEUROTOXICITY SYNDROMES; RECEPTORS, ANTIGEN, T-CELL; TRANSPLANTATION, AUTOLOGOUS;

EID: 85048303785     PISSN: 21598274     EISSN: 21598290     Source Type: Journal    
DOI: 10.1158/2159-8290.CD-17-1368     Document Type: Article

References (41)

1. Park JH, Geyer MB, Brentjens RJ. CD19-targeted CAR T-cell therapeutics for hematologic malignancies: interpreting clinical outcomes to date. Blood 2016;127:3312-20.
2. Maude SL, Teachey DT, Porter DL, Grupp SA. CD19-targeted chimeric antigen receptor T-cell therapy for acute lymphoblastic leukemia. Blood 2015;125:4017-23.
3. Tasian SK, Gardner RA. CD19-redirected chimeric antigen receptormodified T cells: a promising immunotherapy for children and adults with B-cell acute lymphoblastic leukemia (ALL). Ther Adv Hematol 2015;6:228-41.
4. Gardner RA, Finney O, Annesley C, Brakke H, Summers C, Leger K, et al. Intent-to-treat leukemia remission by CD19 CAR T cells of defined formulation and dose in children and young adults. Blood 2017;129:3322-31.
5. Lee DW, Gardner R, Porter DL, Louis CU, Ahmed N, Jensen M, et al. Current concepts in the diagnosis and management of cytokine release syndrome. Blood 2014;124:188-95.
6. 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.
7. Hay KA, HanafiL-A, Li D, Gust J, Liles WC, Wurfel MM, et al. Kinetics and biomarkers of severe cytokine release syndrome after CD19 chimeric antigen receptor-modified T-cell therapy. Blood 2017;130:2295-306.
8. 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 Translat Med 2014;6:224ra25.
9. Maude SL, Barrett D, Teachey DT, Grupp SA. Managing cytokine release syndrome associated with novel T cell-engaging therapies. Cancer J 2014;20:119-22.
10. Bonifant CL, Jackson HJ, Brentjens RJ, Curran KJ. Toxicity and management in CAR T-cell therapy. Mol Ther 2016;3:16011.
11. Brudno JN, Kochenderfer JN. Toxicities of chimeric antigen receptor T cells: recognition and management. Blood 2016;127:3321-30.
12. Gust J, Hay KA, HanafiL-A, Li D, Myerson D, Gonzalez-Cuyar LF, et al. Endothelial activation and blood-brain barrier disruption in neurotoxicity after adoptive immunotherapy with CD19 CAR-T cells. Cancer Discov 2017;7:1404-19.
13. Evans ME, Kumkhaek C, Hsieh MM, Donahue RE, Tisdale JF, Uchida N. TRIM5α variations influence transduction efficiency with lentiviral vectors in both human and rhesus CD34(+) cells in vitro and in vivo. Mol Ther 2014;22:348-58.
14. Uchida N, Hargrove PW, Lap CJ, Evans ME, Phang O, Bonifacino AC, et al. High-efficiency transduction of rhesus hematopoietic repopulating cells by a modified HIV1-based lentiviral vector. Mol Ther 2012;20:1882-92.
15. Hanawa H, Hematti P, Keyvanfar K, Metzger ME, Krouse A, Donahue RE, et al. Efficient gene transfer into rhesus repopulating hematopoietic stem cells using a simian immunodeficiency virus-based lentiviral vector system. Blood 2004;103:4062-9.
16. Jonnalagadda M, Mardiros A, Urak R, Wang X, Hoffman LJ, Bernanke A, et al. Chimeric antigen receptors with mutated IgG4 Fc spacer avoid fc receptor binding and improve T cell persistence and antitumor efficacy. Mol Ther 2015;23:757-68.
17. Wang X, Chang W-C, 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.
18. Sommermeyer D, Hudecek M, Kosasih PL, Gogishvili T, Maloney DG, Turtle CJ, et al. Chimeric antigen receptor-modified T cells derived from defined CD8+ and CD4+ subsets confer superior antitumor reactivity in vivo. Leukemia 2016;30:492-500.
19. Berger C, Jensen MC, Lansdorp PM, Gough M, Elliott C, Riddell SR. Adoptive transfer of effector CD8+ T cells derived from central memory cells establishes persistent T cell memory in primates. J Clin Invest 2008;118:294-305.
20. Berger C, Sommermeyer D, Hudecek M, Berger M, Balakrishnan A, Paszkiewicz PJ, et al. Safety of targeting ROR1 in primates with chimeric antigen receptor-modified T cells. Cancer Immunol Res 2014;3:206-16.
21. Macchia I, Gauduin M-C, Kaur A, Johnson RP. Expression of CD8α identifies a distinct subset of effector memory CD4+ T lymphocytes. Immunology 2006;119:232-42.
22. Lee DW, Kochenderfer JN, Stetler-Stevenson M, Cui YK, Delbrook C, Feldman SA, et al. T cells expressing CD19 chimeric antigen receptors for acute lymphoblastic leukaemia in children and young adults: a phase 1 dose-escalation trial. The Lancet 2015;385:517-28.
23. Engelhardt B. Molecular mechanisms involved in T cell migration across the blood-brain barrier. J Neural Transm (Vienna) 2006;113:477-85.
24. Kranick S, Phan G, Kochenderfer J, Rosenberg S, Nath A. Aphasia as a complication of CD19-targeted chimeric antigen receptor immunotherapy (S52.006). Neurology 2014;82.
25. Reagan PM, Friedberg JW. Reassessment of Anti-CD20 therapy in lymphoid malignancies: impact, limitations, and new directions. Oncology (Williston Park) 2017;31:402-11.
26. Louveau A, Smirnov I, Keyes TJ, Eccles JD, Rouhani SJ, Peske JD, et al. Structural and functional features of central nervous system lymphatic vessels. Nature 2015;523:337-41.
27. Bakken TE, Miller JA, Ding S-L, Sunkin SM, Smith KA, Ng L, et al. A comprehensive transcriptional map of primate brain development. Nature 2016;535:367-75.
28. Tian L, Ma L, Kaarela T, Li Z. Neuroimmune crosstalk in the central nervous system and its significance for neurological diseases. J Neuroinflammation 2012;9:155.
29. da Fonseca ACC, Matias D, Garcia C, Amaral R, Geraldo LH, Freitas C, et al. The impact of microglial activation on blood-brain barrier in brain diseases. Front Cell Neurosci 2014;8:362.
30. Romme Christensen J, Börnsen L, Hesse D, Krakauer M, Sørensen PS, Søndergaard HB, et al. Cellular sources of dysregulated cytokines in relapsing-remitting multiple sclerosis. J Neuroinflamm 2012;9:215.
31. Fragoso-Loyo H, Richaud-Patin Y, Orozco-Narvaez A, Davila-Maldonado L, Atisha-Fregoso Y, Llorente L, et al. Interleukin-6 and chemokines in the neuropsychiatric manifestations of systemic lupus erythematosus. Arthritis Rheum 2007;56:1242-50.
32. Dutcher JP, Schwartzentruber DJ, Kaufman HL, Agarwala SS, Tarhini AA, Lowder JN, et al. High dose interleukin-2 (Aldesleukin)-expert consensus on best management practices-2014. J Immunother Cancer 2014;2:26.
33. Kessing CF, Tyor WR. Interferon-α induces neurotoxicity through activation of the type I receptor and the GluN2A subunit of the NMDA receptor. J Interferon Cytokine Res 2015;35:317-24.
34. Topp MS, Gokbuget N, Stein AS, Zugmaier G, O’Brien S, Bargou RC, 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.
35. Gofton TE, Young GB. Sepsis-associated encephalopathy. Nat Rev Neurol 2012;8:557-66.
36. Wardill HR, Mander KA, Van Sebille YZA, Gibson RJ, Logan RM, Bowen JM, et al. Cytokine-mediated blood-brain barrier disruption as a conduit for cancer/chemotherapy-associated neurotoxicity and cognitive dysfunction. Int J Cancer 2016;139:2635-45.
37. Hudecek M, Sommermeyer D, Kosasih PL, Silva-Benedict A, Liu L, Rader C, et al. The nonsignaling extracellular spacer domain of chimeric antigen receptors is decisive for in vivo antitumor activity. Cancer Immunol Res 2015;3:125-35.
38. Kaur A, Daniel MD, Hempel D, Lee-Parritz D, Hirsch MS, Johnson RP. Cytotoxic T-lymphocyte responses to cytomegalovirus in normal and simian immunodeficiency virus-infected rhesus macaques. J Virol 1996;70:7725-33.
39. 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.
40. Wang J, Jensen M, Lin Y, Sui X, Chen E, Lindgren CG, et al. Optimizing adoptive polyclonal T cell immunotherapy of lymphomas, using a chimeric T cell receptor possessing CD28 and CD137 costimulatory domains. Hum Gene Ther 2007;18:712-25.
41. Pitcher CJ, Hagen SI, Walker JM, Lum R, Mitchell BL, Maino VC, et al. Development and homeostasis of T Cell memory in rhesus macaque. J Immunol 2002;168:29-43.