Frontiers in Immunology (Mar 2020)
Point-Of-Care CAR T-Cell Production (ARI-0001) Using a Closed Semi-automatic Bioreactor: Experience From an Academic Phase I Clinical Trial
- Maria Castella,
- Maria Castella,
- Maria Castella,
- Miguel Caballero-Baños,
- Miguel Caballero-Baños,
- Valentín Ortiz-Maldonado,
- Europa Azucena González-Navarro,
- Guillermo Suñé,
- Guillermo Suñé,
- Asier Antoñana-Vidósola,
- Asier Antoñana-Vidósola,
- Anna Boronat,
- Anna Boronat,
- Berta Marzal,
- Lucía Millán,
- Beatriz Martín-Antonio,
- Beatriz Martín-Antonio,
- Joan Cid,
- Joan Cid,
- Miquel Lozano,
- Miquel Lozano,
- Enric García,
- Enric García,
- Jaime Tabera,
- Jaime Tabera,
- Esteve Trias,
- Unai Perpiña,
- Josep Ma Canals,
- Josep Ma Canals,
- Josep Ma Canals,
- Tycho Baumann,
- Daniel Benítez-Ribas,
- Daniel Benítez-Ribas,
- Elías Campo,
- Elías Campo,
- Elías Campo,
- Elías Campo,
- Elías Campo,
- Jordi Yagüe,
- Jordi Yagüe,
- Jordi Yagüe,
- Álvaro Urbano-Ispizua,
- Álvaro Urbano-Ispizua,
- Álvaro Urbano-Ispizua,
- Álvaro Urbano-Ispizua,
- Álvaro Urbano-Ispizua,
- Susana Rives,
- Susana Rives,
- Julio Delgado,
- Julio Delgado,
- Julio Delgado,
- Julio Delgado,
- Manel Juan,
- Manel Juan,
- Manel Juan,
- Manel Juan,
- Manel Juan,
- Manel Juan
Affiliations
- Maria Castella
- Department of Hematology, Institut Clínic de Malalties Hematològiques i Oncològiques, Hospital Clínic de Barcelona, Barcelona, Spain
- Maria Castella
- Institut D'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain
- Maria Castella
- Blood and Tissue Bank (BST), Barcelona, Spain
- Miguel Caballero-Baños
- Department of Immunology, Centro de Diagnóstico Biomédico, Hospital Clínic de Barcelona, Barcelona, Spain
- Miguel Caballero-Baños
- Hospital Sant Joan de Déu, Barcelona, Spain
- Valentín Ortiz-Maldonado
- Department of Hematology, Institut Clínic de Malalties Hematològiques i Oncològiques, Hospital Clínic de Barcelona, Barcelona, Spain
- Europa Azucena González-Navarro
- Department of Immunology, Centro de Diagnóstico Biomédico, Hospital Clínic de Barcelona, Barcelona, Spain
- Guillermo Suñé
- Department of Hematology, Institut Clínic de Malalties Hematològiques i Oncològiques, Hospital Clínic de Barcelona, Barcelona, Spain
- Guillermo Suñé
- Institut D'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain
- Asier Antoñana-Vidósola
- Department of Hematology, Institut Clínic de Malalties Hematològiques i Oncològiques, Hospital Clínic de Barcelona, Barcelona, Spain
- Asier Antoñana-Vidósola
- Institut D'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain
- Anna Boronat
- Institut D'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain
- Anna Boronat
- Department of Immunology, Centro de Diagnóstico Biomédico, Hospital Clínic de Barcelona, Barcelona, Spain
- Berta Marzal
- Department of Immunology, Centro de Diagnóstico Biomédico, Hospital Clínic de Barcelona, Barcelona, Spain
- Lucía Millán
- Department of Immunology, Centro de Diagnóstico Biomédico, Hospital Clínic de Barcelona, Barcelona, Spain
- Beatriz Martín-Antonio
- Department of Hematology, Institut Clínic de Malalties Hematològiques i Oncològiques, Hospital Clínic de Barcelona, Barcelona, Spain
- Beatriz Martín-Antonio
- Institut D'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain
- Joan Cid
- Institut D'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain
- Joan Cid
- Department of Hemotherapy and Hemostasis, Institut Clínic de Malalties Hematològiques i Oncològiques, Hospital Clínic de Barcelona, Barcelona, Spain
- Miquel Lozano
- Institut D'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain
- Miquel Lozano
- Department of Hemotherapy and Hemostasis, Institut Clínic de Malalties Hematològiques i Oncològiques, Hospital Clínic de Barcelona, Barcelona, Spain
- Enric García
- Blood and Tissue Bank (BST), Barcelona, Spain
- Enric García
- Apheresis Unit, Hospital Sant Joan de Déu de Barcelona, Barcelona, Spain
- Jaime Tabera
- Blood and Tissue Bank (BST), Barcelona, Spain
- Jaime Tabera
- Unit of Advanced Therapies, Hospital Clínic de Barcelona, Barcelona, Spain
- Esteve Trias
- Unit of Advanced Therapies, Hospital Clínic de Barcelona, Barcelona, Spain
- Unai Perpiña
- Stem Cells and Regenerative Medicine Laboratory, Department of Biomedical Sciences, Production and Validation Center of Advanced Therapies (Creatio), Universitat de Barcelona, Barcelona, Spain
- Josep Ma Canals
- Institut D'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain
- Josep Ma Canals
- Stem Cells and Regenerative Medicine Laboratory, Department of Biomedical Sciences, Production and Validation Center of Advanced Therapies (Creatio), Universitat de Barcelona, Barcelona, Spain
- Josep Ma Canals
- 0Universitat de Barcelona, Barcelona, Spain
- Tycho Baumann
- Department of Hematology, Institut Clínic de Malalties Hematològiques i Oncològiques, Hospital Clínic de Barcelona, Barcelona, Spain
- Daniel Benítez-Ribas
- Institut D'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain
- Daniel Benítez-Ribas
- Department of Immunology, Centro de Diagnóstico Biomédico, Hospital Clínic de Barcelona, Barcelona, Spain
- Elías Campo
- Institut D'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain
- Elías Campo
- 0Universitat de Barcelona, Barcelona, Spain
- Elías Campo
- 1Department of Pathology, Hospital Clínic de Barcelona, IDIBAPS, Barcelona, Spain
- Elías Campo
- 2Centro de Investigación Biomedical en Red de Cancer, Barcelona, Spain
- Elías Campo
- 3Institució Catalana de Recerca i Estudis Avancats, Barcelona, Spain
- Jordi Yagüe
- Institut D'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain
- Jordi Yagüe
- Department of Immunology, Centro de Diagnóstico Biomédico, Hospital Clínic de Barcelona, Barcelona, Spain
- Jordi Yagüe
- 0Universitat de Barcelona, Barcelona, Spain
- Álvaro Urbano-Ispizua
- Department of Hematology, Institut Clínic de Malalties Hematològiques i Oncològiques, Hospital Clínic de Barcelona, Barcelona, Spain
- Álvaro Urbano-Ispizua
- Institut D'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain
- Álvaro Urbano-Ispizua
- 0Universitat de Barcelona, Barcelona, Spain
- Álvaro Urbano-Ispizua
- 4Department of Biomedicine, School of Medicine, Josep Carreras Leukemia Research Institute, Universitat de Barcelona, Barcelona, Spain
- Álvaro Urbano-Ispizua
- 5Immunotherapy Unit Blood and Tissue Bank-Hospital Clínic de Barcelona, Barcelona, Spain
- Susana Rives
- 6Department of Pediatric Hematology and Oncology, Hospital Sant Joan de Déu, Barcelona, Spain
- Susana Rives
- 7Institut de Recerca Sant Joan de Déu, Barcelona, Spain
- Julio Delgado
- Department of Hematology, Institut Clínic de Malalties Hematològiques i Oncològiques, Hospital Clínic de Barcelona, Barcelona, Spain
- Julio Delgado
- Institut D'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain
- Julio Delgado
- 0Universitat de Barcelona, Barcelona, Spain
- Julio Delgado
- 2Centro de Investigación Biomedical en Red de Cancer, Barcelona, Spain
- Manel Juan
- Institut D'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain
- Manel Juan
- Blood and Tissue Bank (BST), Barcelona, Spain
- Manel Juan
- Department of Immunology, Centro de Diagnóstico Biomédico, Hospital Clínic de Barcelona, Barcelona, Spain
- Manel Juan
- Hospital Sant Joan de Déu, Barcelona, Spain
- Manel Juan
- 0Universitat de Barcelona, Barcelona, Spain
- Manel Juan
- 5Immunotherapy Unit Blood and Tissue Bank-Hospital Clínic de Barcelona, Barcelona, Spain
- DOI
- https://doi.org/10.3389/fimmu.2020.00482
- Journal volume & issue
-
Vol. 11
Abstract
Development of semi-automated devices that can reduce the hands-on time and standardize the production of clinical-grade CAR T-cells, such as CliniMACS Prodigy from Miltenyi, is key to facilitate the development of CAR T-cell therapies, especially in academic institutions. However, the feasibility of manufacturing CAR T-cell products from heavily pre-treated patients with this system has not been demonstrated yet. Here we report and characterize the production of 28 CAR T-cell products in the context of a phase I clinical trial for CD19+ B-cell malignancies (NCT03144583). The system includes CD4-CD8 cell selection, lentiviral transduction and T-cell expansion using IL-7/IL-15. Twenty-seven out of 28 CAR T-cell products manufactured met the full list of specifications and were considered valid products. Ex vivo cell expansion lasted an average of 8.5 days and had a mean transduction rate of 30.6 ± 13.44%. All products obtained presented cytotoxic activity against CD19+ cells and were proficient in the secretion of pro-inflammatory cytokines. Expansion kinetics was slower in patient's cells compared to healthy donor's cells. However, product potency was comparable. CAR T-cell subset phenotype was highly variable among patients and largely determined by the initial product. TCM and TEM were the predominant T-cell phenotypes obtained. 38.7% of CAR T-cells obtained presented a TN or TCM phenotype, in average, which are the subsets capable of establishing a long-lasting T-cell memory in patients. An in-depth analysis to identify individual factors contributing to the optimal T-cell phenotype revealed that ex vivo cell expansion leads to reduced numbers of TN, TSCM, and TEFF cells, while TCM cells increase, both due to cell expansion and CAR-expression. Overall, our results show for the first time that clinical-grade production of CAR T-cells for heavily pre-treated patients using CliniMACS Prodigy system is feasible, and that the obtained products meet the current quality standards of the field. Reduced ex vivo expansion may yield CAR T-cell products with increased persistence in vivo.
Keywords