CD19 CAR T cell product and disease attributes predict leukemia remission durability
Chimeric antigen receptor (CAR) T cells can induce remission in highly refractory leukemia and lymphoma subjects, yet the parameters for achieving sustained relapse-free survival are not fully delineated. We analyzed 43 pediatric and young adult subjects participating in a Phase I trial of defined c...
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| Published in | The Journal of clinical investigation Vol. 129; no. 5; pp. 2123 - 2132 |
|---|---|
| Main Authors | , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
American Society for Clinical Investigation
01.05.2019
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| Subjects | |
| Online Access | Get full text |
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| Abstract | Chimeric antigen receptor (CAR) T cells can induce remission in highly refractory leukemia and lymphoma subjects, yet the parameters for achieving sustained relapse-free survival are not fully delineated.
We analyzed 43 pediatric and young adult subjects participating in a Phase I trial of defined composition CD19CAR T cells (NCT02028455). CAR T cell phenotype, function and expansion, as well as starting material T cell repertoire, were analyzed in relation to therapeutic outcome (defined as achieving complete remission within 63 days) and duration of leukemia free survival and B cell aplasia.
These analyses reveal that initial therapeutic failures (n = 5) were associated with attenuated CAR T cell expansion and/or rapid attrition of functional CAR effector cells following adoptive transfer. The CAR T products were similar in phenotype and function when compared to products resulting in sustained remissions. However, the initial apheresed peripheral blood T cells could be distinguished by an increased frequency of LAG-3+/TNF-αlow CD8 T cells and, following adoptive transfer, the rapid expression of exhaustion markers. For the 38 subjects who achieved an initial sustained MRD-neg remission, remission durability correlated with therapeutic products having increased frequencies of TNF-α-secreting CAR CD8+ T cells, and was dependent on a sufficiently high CD19+ antigen load at time of infusion to trigger CAR T cell proliferation.
These parameters have the potential to prospectively identify patients at risk for therapeutic failure and support the development of approaches to boost CAR T cell activation and proliferation in patients with low levels of CD19 antigen.
ClinicalTrials.gov NCT02028455.
Partial funding for this study was provided by Stand Up to Cancer & St. Baldrick's Pediatric Dream Team Translational Research Grant (SU2C-AACR-DT1113), RO1 CA136551-05, Alex Lemonade Stand Phase I/II Infrastructure Grant, Conquer Cancer Foundation Career Development Award, Washington State Life Sciences Discovery Fund, Ben Towne Foundation, William Lawrence & Blanche Hughes Foundation, and Juno Therapeutics, Inc., a Celgene Company. |
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| AbstractList | TRIAL REGISTRATION. ClinicalTrials.gov, NCT02028455. BACKGROUND. Chimeric antigen receptor (CAR) T cells can induce remission in highly refractory leukemia and lymphoma subjects, yet the parameters for achieving sustained relapse-free survival are not fully delineated. METHODS. We analyzed 43 pediatric and young adult subjects participating in a phase I trial of defined composition CD19 CAR T cells (ClinicalTrials.gov, NCT02028455). CAR T cell phenotype, function, and expansion, as well as starting material T cell repertoire, were analyzed in relationship to therapeutic outcome (defined as achieving complete remission within 63 days) and duration of leukemia-free survival and B cell aplasia. RESULTS. These analyses reveal that initial therapeutic failures (n = 5) were associated with attenuated CAR T cell expansion and/or rapid attrition of functional CAR effector cells following adoptive transfer. The CAR T products were similar in phenotype and function when compared with products resulting in sustained remissions. However, the initial apheresed peripheral blood T cells could be distinguished by an increased frequency of LAG-3+/TNF-αlo CD8 T cells and, following adoptive transfer, the rapid expression of exhaustion markers. For the 38 subjects who achieved an initial sustained minimal residual disease-negative remission, 15 are still in remission, 10 of whom underwent allogenic hematopoietic stem cell transplantation (alloHSCT) following CAR T treatment. Subsequent remission durability correlated with therapeutic products having increased frequencies of TNF-α-secreting CAR CD8+ T cells, but was dependent on a sufficiently high CD19+ antigen load at time of infusion to trigger CAR T cell proliferation. CONCLUSION. These parameters have the potential to prospectively identify patients at risk for therapeutic failure and support the development of approaches to boost CAR T cell activation and proliferation in patients with low levels of CD19 antigen. Chimeric antigen receptor (CAR) T cells can induce remission in highly refractory leukemia and lymphoma subjects, yet the parameters for achieving sustained relapse-free survival are not fully delineated. We analyzed 43 pediatric and young adult subjects participating in a Phase I trial of defined composition CD19CAR T cells (NCT02028455). CAR T cell phenotype, function and expansion, as well as starting material T cell repertoire, were analyzed in relation to therapeutic outcome (defined as achieving complete remission within 63 days) and duration of leukemia free survival and B cell aplasia. These analyses reveal that initial therapeutic failures (n = 5) were associated with attenuated CAR T cell expansion and/or rapid attrition of functional CAR effector cells following adoptive transfer. The CAR T products were similar in phenotype and function when compared to products resulting in sustained remissions. However, the initial apheresed peripheral blood T cells could be distinguished by an increased frequency of LAG-3+/TNF-αlow CD8 T cells and, following adoptive transfer, the rapid expression of exhaustion markers. For the 38 subjects who achieved an initial sustained MRD-neg remission, remission durability correlated with therapeutic products having increased frequencies of TNF-α-secreting CAR CD8+ T cells, and was dependent on a sufficiently high CD19+ antigen load at time of infusion to trigger CAR T cell proliferation. These parameters have the potential to prospectively identify patients at risk for therapeutic failure and support the development of approaches to boost CAR T cell activation and proliferation in patients with low levels of CD19 antigen. ClinicalTrials.gov NCT02028455. Partial funding for this study was provided by Stand Up to Cancer & St. Baldrick's Pediatric Dream Team Translational Research Grant (SU2C-AACR-DT1113), RO1 CA136551-05, Alex Lemonade Stand Phase I/II Infrastructure Grant, Conquer Cancer Foundation Career Development Award, Washington State Life Sciences Discovery Fund, Ben Towne Foundation, William Lawrence & Blanche Hughes Foundation, and Juno Therapeutics, Inc., a Celgene Company. BACKGROUND. Chimeric antigen receptor (CAR) T cells can induce remission in highly refractory leukemia and lymphoma subjects, yet the parameters for achieving sustained relapse-free survival are not fully delineated. METHODS. We analyzed 43 pediatric and young adult subjects participating in a phase I trial of defined composition CD19 CAR T cells (ClinicalTrials.gov, NCT02028455). CAR T cell phenotype, function, and expansion, as well as starting material T cell repertoire, were analyzed in relationship to therapeutic outcome (defined as achieving complete remission within 63 days) and duration of leukemia-free survival and B cell aplasia. RESULTS. These analyses reveal that initial therapeutic failures (n = 5) were associated with attenuated CAR T cell expansion and/or rapid attrition of functional CAR effector cells following adoptive transfer. The CAR T products were similar in phenotype and function when compared with products resulting in sustained remissions. However, the initial apheresed peripheral blood T cells could be distinguished by an increased frequency of [LAG-3.sup.+]/TNF-[[alpha].sup.lo] CD8 T cells and, following adoptive transfer, the rapid expression of exhaustion markers. For the 38 subjects who achieved an initial sustained minimal residual disease-negative remission, 15 are still in remission, 10 of whom underwent allogenic hematopoietic stem cell transplantation (alloHSCT) following CAR T treatment. Subsequent remission durability correlated with therapeutic products having increased frequencies of TNF-[alpha]-secreting CAR [CD8.sup.+] T cells, but was dependent on a sufficiently high [CD19.sup.+] antigen load at time of infusion to trigger CAR T cell proliferation. CONCLUSION. These parameters have the potential to prospectively identify patients at risk for therapeutic failure and support the development of approaches to boost CAR T cell activation and proliferation in patients with low levels of CD19 antigen. TRIAL REGISTRATION. ClinicalTrials.gov, NCT02028455. FUNDING. Partial funding for this study was provided by a Stand Up to Cancer and St. Baldrick's Pediatric Dream Team Translational Research Grant (SU2C-AACR-DT1113), R01 CA136551-05, an Alex Lemonade Stand Phase I/II Infrastructure Grant, a Conquer Cancer Foundation Career Development Award, the Washington State Life Sciences Discovery Fund, the Ben Towne Foundation, the William Lawrence & Blanche Hughes Foundation, and Juno Therapeutics Inc., a Celgene Company. Chimeric antigen receptor (CAR) T cells can induce remission in highly refractory leukemia and lymphoma subjects, yet the parameters for achieving sustained relapse-free survival are not fully delineated.BACKGROUNDChimeric antigen receptor (CAR) T cells can induce remission in highly refractory leukemia and lymphoma subjects, yet the parameters for achieving sustained relapse-free survival are not fully delineated.We analyzed 43 pediatric and young adult subjects participating in a Phase I trial of defined composition CD19CAR T cells (NCT02028455). CAR T cell phenotype, function and expansion, as well as starting material T cell repertoire, were analyzed in relation to therapeutic outcome (defined as achieving complete remission within 63 days) and duration of leukemia free survival and B cell aplasia.METHODSWe analyzed 43 pediatric and young adult subjects participating in a Phase I trial of defined composition CD19CAR T cells (NCT02028455). CAR T cell phenotype, function and expansion, as well as starting material T cell repertoire, were analyzed in relation to therapeutic outcome (defined as achieving complete remission within 63 days) and duration of leukemia free survival and B cell aplasia.These analyses reveal that initial therapeutic failures (n = 5) were associated with attenuated CAR T cell expansion and/or rapid attrition of functional CAR effector cells following adoptive transfer. The CAR T products were similar in phenotype and function when compared to products resulting in sustained remissions. However, the initial apheresed peripheral blood T cells could be distinguished by an increased frequency of LAG-3+/TNF-αlow CD8 T cells and, following adoptive transfer, the rapid expression of exhaustion markers. For the 38 subjects who achieved an initial sustained MRD-neg remission, remission durability correlated with therapeutic products having increased frequencies of TNF-α-secreting CAR CD8+ T cells, and was dependent on a sufficiently high CD19+ antigen load at time of infusion to trigger CAR T cell proliferation.RESULTSThese analyses reveal that initial therapeutic failures (n = 5) were associated with attenuated CAR T cell expansion and/or rapid attrition of functional CAR effector cells following adoptive transfer. The CAR T products were similar in phenotype and function when compared to products resulting in sustained remissions. However, the initial apheresed peripheral blood T cells could be distinguished by an increased frequency of LAG-3+/TNF-αlow CD8 T cells and, following adoptive transfer, the rapid expression of exhaustion markers. For the 38 subjects who achieved an initial sustained MRD-neg remission, remission durability correlated with therapeutic products having increased frequencies of TNF-α-secreting CAR CD8+ T cells, and was dependent on a sufficiently high CD19+ antigen load at time of infusion to trigger CAR T cell proliferation.These parameters have the potential to prospectively identify patients at risk for therapeutic failure and support the development of approaches to boost CAR T cell activation and proliferation in patients with low levels of CD19 antigen.CONCLUSIONThese parameters have the potential to prospectively identify patients at risk for therapeutic failure and support the development of approaches to boost CAR T cell activation and proliferation in patients with low levels of CD19 antigen.ClinicalTrials.gov NCT02028455.TRIAL REGISTRATIONClinicalTrials.gov NCT02028455.Partial funding for this study was provided by Stand Up to Cancer & St. Baldrick's Pediatric Dream Team Translational Research Grant (SU2C-AACR-DT1113), RO1 CA136551-05, Alex Lemonade Stand Phase I/II Infrastructure Grant, Conquer Cancer Foundation Career Development Award, Washington State Life Sciences Discovery Fund, Ben Towne Foundation, William Lawrence & Blanche Hughes Foundation, and Juno Therapeutics, Inc., a Celgene Company.FUNDINGPartial funding for this study was provided by Stand Up to Cancer & St. Baldrick's Pediatric Dream Team Translational Research Grant (SU2C-AACR-DT1113), RO1 CA136551-05, Alex Lemonade Stand Phase I/II Infrastructure Grant, Conquer Cancer Foundation Career Development Award, Washington State Life Sciences Discovery Fund, Ben Towne Foundation, William Lawrence & Blanche Hughes Foundation, and Juno Therapeutics, Inc., a Celgene Company. BACKGROUND. Chimeric antigen receptor (CAR) T cells can induce remission in highly refractory leukemia and lymphoma subjects, yet the parameters for achieving sustained relapse-free survival are not fully delineated. METHODS. We analyzed 43 pediatric and young adult subjects participating in a phase I trial of defined composition CD19 CAR T cells (ClinicalTrials.gov, NCT02028455). CAR T cell phenotype, function, and expansion, as well as starting material T cell repertoire, were analyzed in relationship to therapeutic outcome (defined as achieving complete remission within 63 days) and duration of leukemia-free survival and B cell aplasia . RESULTS. These analyses reveal that initial therapeutic failures ( n = 5) were associated with attenuated CAR T cell expansion and/or rapid attrition of functional CAR effector cells following adoptive transfer. The CAR T products were similar in phenotype and function when compared with products resulting in sustained remissions. However, the initial apheresed peripheral blood T cells could be distinguished by an increased frequency of LAG-3 + /TNF- α lo CD8 T cells and, following adoptive transfer, the rapid expression of exhaustion markers. For the 38 subjects who achieved an initial sustained minimal residual disease–negative remission, 15 are still in remission, 10 of whom underwent allogenic hematopoietic stem cell transplantation (alloHSCT) following CAR T treatment. Subsequent remission durability correlated with therapeutic products having increased frequencies of TNF- α –secreting CAR CD8 + T cells, but was dependent on a sufficiently high CD19 + antigen load at time of infusion to trigger CAR T cell proliferation. CONCLUSION. These parameters have the potential to prospectively identify patients at risk for therapeutic failure and support the development of approaches to boost CAR T cell activation and proliferation in patients with low levels of CD19 antigen. TRIAL REGISTRATION. ClinicalTrials.gov, NCT02028455. FUNDING. Partial funding for this study was provided by a Stand Up to Cancer and St. Baldrick’s Pediatric Dream Team Translational Research Grant (SU2C-AACR-DT1113), R01 CA136551-05, an Alex Lemonade Stand Phase I/II Infrastructure Grant, a Conquer Cancer Foundation Career Development Award, the Washington State Life Sciences Discovery Fund, the Ben Towne Foundation, the William Lawrence & Blanche Hughes Foundation, and Juno Therapeutics Inc., a Celgene Company. |
| Audience | Academic |
| Author | Finney, Olivia C. Lopez, Marisa Hicks, Roxana Doolittle, Danielle Futrell, Ben Jensen, Michael C. Brakke, Hannah Orentas, Rimas J. Gardner, Rebecca Rawlings-Rhea, Stephanie Li, Daniel |
| AuthorAffiliation | 3 Department of Pediatrics, University of Washington, Seattle, Washington, USA 4 Center for Clinical and Translational Research, Seattle Children’s Research Institute, Seattle, Washington, USA 1 Ben Towne Center for Childhood Cancer Research, Seattle Children’s Research Institute, Seattle, Washington, USA 5 Clinical Research Division, Fred Hutchinson Cancer Research Center, Seattle, Washington, USA 2 Clinical Statistics Group, Juno Therapeutics, Inc., Seattle, Washington, USA |
| AuthorAffiliation_xml | – name: 4 Center for Clinical and Translational Research, Seattle Children’s Research Institute, Seattle, Washington, USA – name: 5 Clinical Research Division, Fred Hutchinson Cancer Research Center, Seattle, Washington, USA – name: 1 Ben Towne Center for Childhood Cancer Research, Seattle Children’s Research Institute, Seattle, Washington, USA – name: 3 Department of Pediatrics, University of Washington, Seattle, Washington, USA – name: 2 Clinical Statistics Group, Juno Therapeutics, Inc., Seattle, Washington, USA |
| Author_xml | – sequence: 1 givenname: Olivia C. surname: Finney fullname: Finney, Olivia C. – sequence: 2 givenname: Hannah surname: Brakke fullname: Brakke, Hannah – sequence: 3 givenname: Stephanie surname: Rawlings-Rhea fullname: Rawlings-Rhea, Stephanie – sequence: 4 givenname: Roxana surname: Hicks fullname: Hicks, Roxana – sequence: 5 givenname: Danielle surname: Doolittle fullname: Doolittle, Danielle – sequence: 6 givenname: Marisa surname: Lopez fullname: Lopez, Marisa – sequence: 7 givenname: Ben surname: Futrell fullname: Futrell, Ben – sequence: 8 givenname: Rimas J. orcidid: 0000-0002-6310-3467 surname: Orentas fullname: Orentas, Rimas J. – sequence: 9 givenname: Daniel surname: Li fullname: Li, Daniel – sequence: 10 givenname: Rebecca surname: Gardner fullname: Gardner, Rebecca – sequence: 11 givenname: Michael C. surname: Jensen fullname: Jensen, Michael C. |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30860496$$D View this record in MEDLINE/PubMed |
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| SubjectTerms | Adolescent Adoptive transfer Adult Antigens Antigens, CD - metabolism Antigens, CD19 - metabolism Aplasia Biomedical research Bone marrow Cancer therapies Care and treatment CD19 antigen CD223 antigen CD8 antigen CD8-Positive T-Lymphocytes - cytology Cell activation Cell Proliferation Cell survival Chemotherapy Child Child, Preschool Chimeric antigen receptors Clinical Medicine Clinical trials Disease-Free Survival Effector cells Failure Female Gene Expression Regulation, Leukemic Hematopoietic Stem Cell Transplantation Hematopoietic stem cells Hepatitis A Virus Cellular Receptor 2 - metabolism Humans Immunophenotyping Immunotherapy Immunotherapy, Adoptive Infant Influenza K562 Cells Kaplan-Meier Estimate Leukemia Leukemia - immunology Leukemia - therapy Lymphocyte Activation Lymphocyte Activation Gene 3 Protein Lymphocytes Lymphocytes B Lymphocytes T Lymphoma Male Medical research Medicine, Experimental Minimal residual disease Patients Pediatrics Peripheral blood Phenotype Phenotypes Programmed Cell Death 1 Receptor - metabolism Receptors, Chimeric Antigen - metabolism Recurrence Remission Remission (Medicine) Remission Induction Stem cell transplantation Stem cells Survival analysis T cells Tumor Necrosis Factor-alpha - metabolism Tumor necrosis factor-α Young Adult Young adults |
| Title | CD19 CAR T cell product and disease attributes predict leukemia remission durability |
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