Off-the-shelf, steroid-resistant, IL13Rα2-specific CAR T cells for treatment of glioblastoma.


Journal

Neuro-oncology
ISSN: 1523-5866
Titre abrégé: Neuro Oncol
Pays: England
ID NLM: 100887420

Informations de publication

Date de publication:
01 08 2022
Historique:
pubmed: 1 2 2022
medline: 3 8 2022
entrez: 31 1 2022
Statut: ppublish

Résumé

Wide-spread application of chimeric antigen receptor (CAR) T cell therapy for cancer is limited by the current use of autologous CAR T cells necessitating the manufacture of individualized therapeutic products for each patient. To address this challenge, we have generated an off-the-shelf, allogeneic CAR T cell product for the treatment of glioblastoma (GBM), and present here the feasibility, safety, and therapeutic potential of this approach. We generated for clinical use a healthy-donor derived IL13Rα2-targeted CAR+ (IL13-zetakine+) cytolytic T-lymphocyte (CTL) product genetically engineered using zinc finger nucleases (ZFNs) to permanently disrupt the glucocorticoid receptor (GR) (GRm13Z40-2) and endow resistance to glucocorticoid treatment. In a phase I safety and feasibility trial we evaluated these allogeneic GRm13Z40-2 T cells in combination with intracranial administration of recombinant human IL-2 (rhIL-2; aldesleukin) in six patients with unresectable recurrent GBM that were maintained on systemic dexamethasone (4-12 mg/day). The GRm13Z40-2 product displayed dexamethasone-resistant effector activity without evidence for in vitro alloreactivity. Intracranial administration of GRm13Z40-2 in four doses of 108 cells over a two-week period with aldesleukin (9 infusions ranging from 2500-5000 IU) was well tolerated, with indications of transient tumor reduction and/or tumor necrosis at the site of T cell infusion in four of the six treated research subjects. Antibody reactivity against GRm13Z40-2 cells was detected in the serum of only one of the four tested subjects. This first-in-human experience establishes a foundation for future adoptive therapy studies using off-the-shelf, zinc-finger modified, and/or glucocorticoid resistant CAR T cells.

Sections du résumé

BACKGROUND
Wide-spread application of chimeric antigen receptor (CAR) T cell therapy for cancer is limited by the current use of autologous CAR T cells necessitating the manufacture of individualized therapeutic products for each patient. To address this challenge, we have generated an off-the-shelf, allogeneic CAR T cell product for the treatment of glioblastoma (GBM), and present here the feasibility, safety, and therapeutic potential of this approach.
METHODS
We generated for clinical use a healthy-donor derived IL13Rα2-targeted CAR+ (IL13-zetakine+) cytolytic T-lymphocyte (CTL) product genetically engineered using zinc finger nucleases (ZFNs) to permanently disrupt the glucocorticoid receptor (GR) (GRm13Z40-2) and endow resistance to glucocorticoid treatment. In a phase I safety and feasibility trial we evaluated these allogeneic GRm13Z40-2 T cells in combination with intracranial administration of recombinant human IL-2 (rhIL-2; aldesleukin) in six patients with unresectable recurrent GBM that were maintained on systemic dexamethasone (4-12 mg/day).
RESULTS
The GRm13Z40-2 product displayed dexamethasone-resistant effector activity without evidence for in vitro alloreactivity. Intracranial administration of GRm13Z40-2 in four doses of 108 cells over a two-week period with aldesleukin (9 infusions ranging from 2500-5000 IU) was well tolerated, with indications of transient tumor reduction and/or tumor necrosis at the site of T cell infusion in four of the six treated research subjects. Antibody reactivity against GRm13Z40-2 cells was detected in the serum of only one of the four tested subjects.
CONCLUSIONS
This first-in-human experience establishes a foundation for future adoptive therapy studies using off-the-shelf, zinc-finger modified, and/or glucocorticoid resistant CAR T cells.

Identifiants

pubmed: 35100373
pii: 6518100
doi: 10.1093/neuonc/noac024
pmc: PMC9340633
doi:

Substances chimiques

Glucocorticoids 0
Interleukin-13 Receptor alpha2 Subunit 0
Steroids 0
Dexamethasone 7S5I7G3JQL

Types de publication

Clinical Trial, Phase I Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

1318-1330

Subventions

Organisme : NCI NIH HHS
ID : P30 CA033572
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA155769
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA236500
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA254271
Pays : United States

Informations de copyright

Published by Oxford University Press on behalf of the Society for Neuro-Oncology 2022.

Références

Cell Rep. 2021 Nov 9;37(6):109992
pubmed: 34758319
N Engl J Med. 2016 Dec 29;375(26):2561-9
pubmed: 28029927
Nature. 2019 Jan;565(7738):234-239
pubmed: 30568305
J Clin Endocrinol Metab. 2003 May;88(5):2309-17
pubmed: 12727990
Mol Ther. 2018 Jan 3;26(1):31-44
pubmed: 29103912
J Immunother. 2011 Mar;34(2):212-20
pubmed: 21304398
Mol Ther. 2000 Jan;1(1):49-55
pubmed: 10933911
Sci Transl Med. 2017 Jan 18;9(373):
pubmed: 28100832
Mol Ther. 2015 Apr;23(4):757-68
pubmed: 25366031
Prog Brain Res. 2010;182:1-30
pubmed: 20541659
Nat Commun. 2020 Jul 15;11(1):3549
pubmed: 32669548
Nucleic Acids Res. 2016 Feb 18;44(3):e30
pubmed: 26527725
Cancer Discov. 2021 Sep;11(9):2248-2265
pubmed: 33837065
N Engl J Med. 2018 Feb 1;378(5):439-448
pubmed: 29385370
Br J Exp Pathol. 1948 Feb;29(1):58-69
pubmed: 18865105
Nat Rev Drug Discov. 2020 Mar;19(3):185-199
pubmed: 31900462
Immunol Rev. 2019 Jul;290(1):60-84
pubmed: 31355493
Annu Rev Biochem. 2007;76:51-74
pubmed: 17352659
Clin Dev Immunol. 2011;2011:732413
pubmed: 22190972
Front Immunol. 2019 Jan 22;9:3062
pubmed: 30740109
Clin Cancer Res. 2015 Sep 15;21(18):4062-72
pubmed: 26059190
Blood. 2012 Jun 14;119(24):5697-705
pubmed: 22535661
Nat Biotechnol. 2013 Oct;31(10):928-33
pubmed: 23934177
Front Oncol. 2018 Sep 27;8:414
pubmed: 30319977
N Engl J Med. 2017 Dec 28;377(26):2531-2544
pubmed: 29226797
Clin Cancer Res. 2021 Jan 1;27(1):276-287
pubmed: 33239433
Science. 2020 Feb 28;367(6481):
pubmed: 32029687
Nature. 1981 Jan 22;289(5795):300-1
pubmed: 6256660
N Engl J Med. 2008 Jun 19;358(25):2698-703
pubmed: 18565862
Front Immunol. 2020 Aug 07;11:1965
pubmed: 32903482

Auteurs

Christine E Brown (CE)

Department of Hematology & Hematopoietic Cell Transplantation (T Cell Therapeutics Research Laboratories), City of Hope Beckman Research Institute and Medical Center; Duarte, California, USA.

Analiz Rodriguez (A)

Department of Neurosurgery, City of Hope Beckman Research Institute and Medical Center; Duarte, California, USA.

Joycelynne Palmer (J)

Department of Computational and Quantitative Medicine, City of Hope Beckman Research Institute and Medical Center; Duarte, California, USA.

Julie R Ostberg (JR)

Department of Hematology & Hematopoietic Cell Transplantation (T Cell Therapeutics Research Laboratories), City of Hope Beckman Research Institute and Medical Center; Duarte, California, USA.

Araceli Naranjo (A)

Department of Hematology & Hematopoietic Cell Transplantation (T Cell Therapeutics Research Laboratories), City of Hope Beckman Research Institute and Medical Center; Duarte, California, USA.

Jamie R Wagner (JR)

Department of Hematology & Hematopoietic Cell Transplantation (T Cell Therapeutics Research Laboratories), City of Hope Beckman Research Institute and Medical Center; Duarte, California, USA.

Brenda Aguilar (B)

Department of Hematology & Hematopoietic Cell Transplantation (T Cell Therapeutics Research Laboratories), City of Hope Beckman Research Institute and Medical Center; Duarte, California, USA.

Renate Starr (R)

Department of Hematology & Hematopoietic Cell Transplantation (T Cell Therapeutics Research Laboratories), City of Hope Beckman Research Institute and Medical Center; Duarte, California, USA.

Lihong Weng (L)

Department of Hematology & Hematopoietic Cell Transplantation (T Cell Therapeutics Research Laboratories), City of Hope Beckman Research Institute and Medical Center; Duarte, California, USA.

Timothy W Synold (TW)

Department of Cancer Biology, City of Hope Beckman Research Institute and Medical Center; Duarte, California, USA.

Vivi Tran (V)

Department of Cancer Biology, City of Hope Beckman Research Institute and Medical Center; Duarte, California, USA.

Shelley Wang (S)

Sangamo Therapeutics, Inc., Richmond, California, USA.

Andreas Reik (A)

Sangamo Therapeutics, Inc., Richmond, California, USA.

Massimo D'Apuzzo (M)

Department of Pathology, City of Hope Beckman Research Institute and Medical Center; Duarte, California, USA.

Julie A Ressler (JA)

Department of Diagnostic Radiology, City of Hope Beckman Research Institute and Medical Center; Duarte, California, USA.

Yuanyue Zhou (Y)

Sangamo Therapeutics, Inc., Richmond, California, USA.

Matthew Mendel (M)

Sangamo Therapeutics, Inc., Richmond, California, USA.

Philip D Gregory (PD)

Sangamo Therapeutics, Inc., Richmond, California, USA.

Michael C Holmes (MC)

Sangamo Therapeutics, Inc., Richmond, California, USA.

Winson W Tang (WW)

Sangamo Therapeutics, Inc., Richmond, California, USA.

Stephen J Forman (SJ)

Department of Hematology & Hematopoietic Cell Transplantation (T Cell Therapeutics Research Laboratories), City of Hope Beckman Research Institute and Medical Center; Duarte, California, USA.

Michael C Jensen (MC)

Ben Town Center for Childhood Cancer, Seattle Children's Research Institute, Seattle, Washington, USA.

Behnam Badie (B)

Department of Neurosurgery, City of Hope Beckman Research Institute and Medical Center; Duarte, California, USA.

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