Determinants of response and resistance to CD19 chimeric antigen receptor (CAR) T cell therapy of chronic lymphocytic leukemia
Tolerance to self-antigens prevents the elimination of cancer by the immune system . We used synthetic chimeric antigen receptors (CARs) to overcome immunological tolerance and mediate tumor rejection in patients with chronic lymphocytic leukemia (CLL). Remission was induced in a subset of subjects,...
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| Published in | Nature medicine Vol. 24; no. 5; pp. 563 - 571 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Nature Publishing Group
01.05.2018
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| Subjects | |
| Online Access | Get full text |
| ISSN | 1078-8956 1546-170X |
| DOI | 10.1038/s41591-018-0010-1 |
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| Abstract | Tolerance to self-antigens prevents the elimination of cancer by the immune system
. We used synthetic chimeric antigen receptors (CARs) to overcome immunological tolerance and mediate tumor rejection in patients with chronic lymphocytic leukemia (CLL). Remission was induced in a subset of subjects, but most did not respond. Comprehensive assessment of patient-derived CAR T cells to identify mechanisms of therapeutic success and failure has not been explored. We performed genomic, phenotypic and functional evaluations to identify determinants of response. Transcriptomic profiling revealed that CAR T cells from complete-responding patients with CLL were enriched in memory-related genes, including IL-6/STAT3 signatures, whereas T cells from nonresponders upregulated programs involved in effector differentiation, glycolysis, exhaustion and apoptosis. Sustained remission was associated with an elevated frequency of CD27
CD45RO
CD8
T cells before CAR T cell generation, and these lymphocytes possessed memory-like characteristics. Highly functional CAR T cells from patients produced STAT3-related cytokines, and serum IL-6 correlated with CAR T cell expansion. IL-6/STAT3 blockade diminished CAR T cell proliferation. Furthermore, a mechanistically relevant population of CD27
PD-1
CD8
CAR T cells expressing high levels of the IL-6 receptor predicts therapeutic response and is responsible for tumor control. These findings uncover new features of CAR T cell biology and underscore the potential of using pretreatment biomarkers of response to advance immunotherapies. |
|---|---|
| AbstractList | Tolerance to self-antigens prevents the elimination of cancer by the immune system1,2. We used synthetic chimeric antigen receptors (CARs) to overcome immunological tolerance and mediate tumor rejection in patients with chronic lymphocytic leukemia (CLL). Remission was induced in a subset of subjects, but most did not respond. Comprehensive assessment of patient-derived CAR T cells to identify mechanisms of therapeutic success and failure has not been explored. We performed genomic, phenotypic and functional evaluations to identify determinants of response. Transcriptomic profiling revealed that CAR T cells from complete-responding patients with CLL were enriched in memory-related genes, including IL-6/STAT3 signatures, whereas T cells from nonresponders upregulated programs involved in effector differentiation, glycolysis, exhaustion and apoptosis. Sustained remission was associated with an elevated frequency of CD27+CD45RO–CD8+ T cells before CAR T cell generation, and these lymphocytes possessed memory-like characteristics. Highly functional CAR T cells from patients produced STAT3-related cytokines, and serum IL-6 correlated with CAR T cell expansion. IL-6/STAT3 blockade diminished CAR T cell proliferation. Furthermore, a mechanistically relevant population of CD27+PD-1–CD8+ CAR T cells expressing high levels of the IL-6 receptor predicts therapeutic response and is responsible for tumor control. These findings uncover new features of CAR T cell biology and underscore the potential of using pretreatment biomarkers of response to advance immunotherapies. Tolerance to self-antigens prevents the elimination of cancer by the immune system . We used synthetic chimeric antigen receptors (CARs) to overcome immunological tolerance and mediate tumor rejection in patients with chronic lymphocytic leukemia (CLL). Remission was induced in a subset of subjects, but most did not respond. Comprehensive assessment of patient-derived CAR T cells to identify mechanisms of therapeutic success and failure has not been explored. We performed genomic, phenotypic and functional evaluations to identify determinants of response. Transcriptomic profiling revealed that CAR T cells from complete-responding patients with CLL were enriched in memory-related genes, including IL-6/STAT3 signatures, whereas T cells from nonresponders upregulated programs involved in effector differentiation, glycolysis, exhaustion and apoptosis. Sustained remission was associated with an elevated frequency of CD27 CD45RO CD8 T cells before CAR T cell generation, and these lymphocytes possessed memory-like characteristics. Highly functional CAR T cells from patients produced STAT3-related cytokines, and serum IL-6 correlated with CAR T cell expansion. IL-6/STAT3 blockade diminished CAR T cell proliferation. Furthermore, a mechanistically relevant population of CD27 PD-1 CD8 CAR T cells expressing high levels of the IL-6 receptor predicts therapeutic response and is responsible for tumor control. These findings uncover new features of CAR T cell biology and underscore the potential of using pretreatment biomarkers of response to advance immunotherapies. Tolerance to self-antigens prevents the elimination of cancer by the immune system1,2. We used synthetic chimeric antigen receptors (CARs) to overcome immunological tolerance and mediate tumor rejection in patients with chronic lymphocytic leukemia (CLL). Remission was induced in a subset of subjects, but most did not respond. Comprehensive assessment of patient-derived CAR T cells to identify mechanisms of therapeutic success and failure has not been explored. We performed genomic, phenotypic and functional evaluations to identify determinants of response. Transcriptomic profiling revealed that CAR T cells from complete-responding patients with CLL were enriched in memory-related genes, including IL-6/STAT3 signatures, whereas T cells from nonresponders upregulated programs involved in effector differentiation, glycolysis, exhaustion and apoptosis. Sustained remission was associated with an elevated frequency of CD27+CD45RO–CD8+ T cells before CAR T cell generation, and these lymphocytes possessed memory-like characteristics. Highly functional CAR T cells from patients produced STAT3-related cytokines, and serum IL-6 correlated with CAR T cell expansion. IL-6/STAT3 blockade diminished CAR T cell proliferation. Furthermore, a mechanistically relevant population of CD27+PD-1–CD8+ CAR T cells expressing high levels of the IL-6 receptor predicts therapeutic response and is responsible for tumor control. These findings uncover new features of CAR T cell biology and underscore the potential of using pretreatment biomarkers of response to advance immunotherapies.An IL-6/STAT3 signature and memory CD8 T cell subset in preinfusion chimeric antigen receptor–expressing T cells associate with response in patients with high-risk chronic lymphocytic leukemia. |
| Author | Kassim, Sadik H Liu, Li Davis, Megan M O'Connor, Roddy S Wilcox, Nicholas Zhang, Changfeng Wherry, E John Gupta, Minnal Frey, Noelle V Wang, Yan Young, Regina M Pruteanu-Malinici, Iulian Dorfmeier, Corin Siegel, Donald L Kulikovskaya, Irina Johnson, F Brad Bitter, Hans Fraietta, Joseph A Boesteanu, Alina C Huang, Alexander C Lundh, Stefan Brogdon, Jennifer L Pequignot, Edward Levine, Bruce L Orlando, Elena J Parakandi, Harit Melenhorst, J Joseph Chen, Fang Xu, Jun Lacey, Simon F Porter, David L Gohil, Mercy Ambrose, David E Bedoya, Felipe Hwang, Wei-Ting June, Carl H Tian, Lifeng |
| Author_xml | – sequence: 1 givenname: Joseph A surname: Fraietta fullname: Fraietta, Joseph A organization: Parker Institute for Cancer Immunotherapy at University of Pennsylvania, Philadelphia, PA, USA – sequence: 2 givenname: Simon F surname: Lacey fullname: Lacey, Simon F organization: Parker Institute for Cancer Immunotherapy at University of Pennsylvania, Philadelphia, PA, USA – sequence: 3 givenname: Elena J surname: Orlando fullname: Orlando, Elena J organization: Novartis Institutes for BioMedical Research, Cambridge, MA, USA – sequence: 4 givenname: Iulian surname: Pruteanu-Malinici fullname: Pruteanu-Malinici, Iulian organization: Novartis Institutes for BioMedical Research, Cambridge, MA, USA – sequence: 5 givenname: Mercy surname: Gohil fullname: Gohil, Mercy organization: Center for Cellular Immunotherapies, University of Pennsylvania, Philadelphia, PA, USA – sequence: 6 givenname: Stefan surname: Lundh fullname: Lundh, Stefan organization: Center for Cellular Immunotherapies, University of Pennsylvania, Philadelphia, PA, USA – sequence: 7 givenname: Alina C surname: Boesteanu fullname: Boesteanu, Alina C organization: Center for Cellular Immunotherapies, University of Pennsylvania, Philadelphia, PA, USA – sequence: 8 givenname: Yan surname: Wang fullname: Wang, Yan organization: Center for Cellular Immunotherapies, University of Pennsylvania, Philadelphia, PA, USA – sequence: 9 givenname: Roddy S surname: O'Connor fullname: O'Connor, Roddy S organization: Center for Cellular Immunotherapies, University of Pennsylvania, Philadelphia, PA, USA – sequence: 10 givenname: Wei-Ting surname: Hwang fullname: Hwang, Wei-Ting organization: Department of Biostatistics and Epidemiology, University of Pennsylvania, Philadelphia, PA, USA – sequence: 11 givenname: Edward surname: Pequignot fullname: Pequignot, Edward organization: Center for Cellular Immunotherapies, University of Pennsylvania, Philadelphia, PA, USA – sequence: 12 givenname: David E surname: Ambrose fullname: Ambrose, David E organization: Center for Cellular Immunotherapies, University of Pennsylvania, Philadelphia, PA, USA – sequence: 13 givenname: Changfeng surname: Zhang fullname: Zhang, Changfeng organization: Center for Cellular Immunotherapies, University of Pennsylvania, Philadelphia, PA, USA – sequence: 14 givenname: Nicholas surname: Wilcox fullname: Wilcox, Nicholas organization: Center for Cellular Immunotherapies, University of Pennsylvania, Philadelphia, PA, USA – sequence: 15 givenname: Felipe surname: Bedoya fullname: Bedoya, Felipe organization: Center for Cellular Immunotherapies, University of Pennsylvania, Philadelphia, PA, USA – sequence: 16 givenname: Corin surname: Dorfmeier fullname: Dorfmeier, Corin organization: Center for Cellular Immunotherapies, University of Pennsylvania, Philadelphia, PA, USA – sequence: 17 givenname: Fang surname: Chen fullname: Chen, Fang organization: Center for Cellular Immunotherapies, University of Pennsylvania, Philadelphia, PA, USA – sequence: 18 givenname: Lifeng surname: Tian fullname: Tian, Lifeng organization: Center for Cellular Immunotherapies, University of Pennsylvania, Philadelphia, PA, USA – sequence: 19 givenname: Harit surname: Parakandi fullname: Parakandi, Harit organization: Center for Cellular Immunotherapies, University of Pennsylvania, Philadelphia, PA, USA – sequence: 20 givenname: Minnal surname: Gupta fullname: Gupta, Minnal organization: Center for Cellular Immunotherapies, University of Pennsylvania, Philadelphia, PA, USA – sequence: 21 givenname: Regina M surname: Young fullname: Young, Regina M organization: Center for Cellular Immunotherapies, University of Pennsylvania, Philadelphia, PA, USA – sequence: 22 givenname: F Brad orcidid: 0000-0002-7443-7227 surname: Johnson fullname: Johnson, F Brad organization: Department of Pathology and Laboratory Medicine, University of Pennsylvania, Philadelphia, PA, USA – sequence: 23 givenname: Irina surname: Kulikovskaya fullname: Kulikovskaya, Irina organization: Center for Cellular Immunotherapies, University of Pennsylvania, Philadelphia, PA, USA – sequence: 24 givenname: Li surname: Liu fullname: Liu, Li organization: Center for Cellular Immunotherapies, University of Pennsylvania, Philadelphia, PA, USA – sequence: 25 givenname: Jun orcidid: 0000-0001-6969-0693 surname: Xu fullname: Xu, Jun organization: Center for Cellular Immunotherapies, University of Pennsylvania, Philadelphia, PA, USA – sequence: 26 givenname: Sadik H surname: Kassim fullname: Kassim, Sadik H organization: Novartis Institutes for BioMedical Research, Cambridge, MA, USA – sequence: 27 givenname: Megan M surname: Davis fullname: Davis, Megan M organization: Center for Cellular Immunotherapies, University of Pennsylvania, Philadelphia, PA, USA – sequence: 28 givenname: Bruce L orcidid: 0000-0001-6971-8465 surname: Levine fullname: Levine, Bruce L organization: Center for Cellular Immunotherapies, University of Pennsylvania, Philadelphia, PA, USA – sequence: 29 givenname: Noelle V surname: Frey fullname: Frey, Noelle V organization: Division of Hematology-Oncology, Department of Internal Medicine, University of Pennsylvania, Philadelphia, PA, USA – sequence: 30 givenname: Donald L surname: Siegel fullname: Siegel, Donald L organization: Division of Transfusion Medicine and Therapeutic Pathology, University of Pennsylvania, Philadelphia, PA, USA – sequence: 31 givenname: Alexander C surname: Huang fullname: Huang, Alexander C organization: Department of Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA – sequence: 32 givenname: E John surname: Wherry fullname: Wherry, E John organization: Department of Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA – sequence: 33 givenname: Hans surname: Bitter fullname: Bitter, Hans organization: Novartis Institutes for BioMedical Research, Cambridge, MA, USA – sequence: 34 givenname: Jennifer L surname: Brogdon fullname: Brogdon, Jennifer L organization: Novartis Institutes for BioMedical Research, Cambridge, MA, USA – sequence: 35 givenname: David L surname: Porter fullname: Porter, David L organization: Division of Hematology-Oncology, Department of Internal Medicine, University of Pennsylvania, Philadelphia, PA, USA – sequence: 36 givenname: Carl H orcidid: 0000-0003-0241-3557 surname: June fullname: June, Carl H organization: Parker Institute for Cancer Immunotherapy at University of Pennsylvania, Philadelphia, PA, USA – sequence: 37 givenname: J Joseph surname: Melenhorst fullname: Melenhorst, J Joseph email: mej@upenn.edu, mej@upenn.edu, mej@upenn.edu organization: Parker Institute for Cancer Immunotherapy at University of Pennsylvania, Philadelphia, PA, USA. mej@upenn.edu |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/29713085$$D View this record in MEDLINE/PubMed |
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| References | 30149852 - Trends Mol Med. 2018 Sep;24(9):729-731 33547459 - Nat Med. 2021 Feb 5 29760506 - Nat Rev Clin Oncol. 2018 Jul;15(7):402-403 29769184 - Cancer Discov. 2018 Jul;8(7):784-785 |
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| Snippet | Tolerance to self-antigens prevents the elimination of cancer by the immune system
. We used synthetic chimeric antigen receptors (CARs) to overcome... Tolerance to self-antigens prevents the elimination of cancer by the immune system1,2. We used synthetic chimeric antigen receptors (CARs) to overcome... |
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| SubjectTerms | Animals Antigens Antigens, CD19 - metabolism Apoptosis Autoantigens Biomarkers Cancer CD19 antigen CD27 antigen CD8 antigen Cell proliferation Cell therapy Chimeric antigen receptors Chronic lymphocytic leukemia Cytokines Exhaustion Female Genomics Glycolysis Immunological memory Immunological tolerance Immunology Immunotherapy Immunotherapy, Adoptive Interleukin 6 Interleukin 6 receptors Interleukin-6 - metabolism Leukemia Leukemia, Lymphocytic, Chronic, B-Cell - immunology Leukemia, Lymphocytic, Chronic, B-Cell - therapy Lymphatic leukemia Lymphocytes Lymphocytes T Male Memory cells Mice Patients PD-1 protein Receptors Receptors, Chimeric Antigen - metabolism Remission Stat3 protein STAT3 Transcription Factor - metabolism Transcription, Genetic Treatment Outcome Tumors |
| Title | Determinants of response and resistance to CD19 chimeric antigen receptor (CAR) T cell therapy of chronic lymphocytic leukemia |
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