Co-opting signalling molecules enables logic-gated control of CAR T cells
Although chimeric antigen receptor (CAR) T cells have altered the treatment landscape for B cell malignancies, the risk of on-target, off-tumour toxicity has hampered their development for solid tumours because most target antigens are shared with normal cells 1 , 2 . Researchers have attempted to a...
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| Published in | Nature (London) Vol. 615; no. 7952; pp. 507 - 516 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
16.03.2023
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
| ISSN | 0028-0836 1476-4687 1476-4687 |
| DOI | 10.1038/s41586-023-05778-2 |
Cover
| Abstract | Although chimeric antigen receptor (CAR) T cells have altered the treatment landscape for B cell malignancies, the risk of on-target, off-tumour toxicity has hampered their development for solid tumours because most target antigens are shared with normal cells
1
,
2
. Researchers have attempted to apply Boolean-logic gating to CAR T cells to prevent toxicity
3
–
5
; however, a truly safe and effective logic-gated CAR has remained elusive
6
. Here we describe an approach to CAR engineering in which we replace traditional CD3ζ domains with intracellular proximal T cell signalling molecules. We show that certain proximal signalling CARs, such as a ZAP-70 CAR, can activate T cells and eradicate tumours in vivo while bypassing upstream signalling proteins, including CD3ζ. The primary role of ZAP-70 is to phosphorylate LAT and SLP-76, which form a scaffold for signal propagation. We exploited the cooperative role of LAT and SLP-76 to engineer logic-gated intracellular network (LINK) CAR, a rapid and reversible Boolean-logic AND-gated CAR T cell platform that outperforms other systems in both efficacy and prevention of on-target, off-tumour toxicity. LINK CAR will expand the range of molecules that can be targeted with CAR T cells, and will enable these powerful therapeutic agents to be used for solid tumours and diverse diseases such as autoimmunity
7
and fibrosis
8
. In addition, this work shows that the internal signalling machinery of cells can be repurposed into surface receptors, which could open new avenues for cellular engineering.
Logic gating is used to develop a CAR T cell platform that is highly specific and allows the activity of T cells to be restricted to the encounter of two antigens, thus reducing on-target, off-tumour toxicity. |
|---|---|
| AbstractList | Although chimeric antigen receptor (CAR) T cells have altered the treatment landscape for B cell malignancies, the risk of on-target, off-tumour toxicity has hampered their development for solid tumours because most target antigens are shared with normal cells
1
,
2
. Researchers have attempted to apply Boolean-logic gating to CAR T cells to prevent toxicity
3
–
5
; however, a truly safe and effective logic-gated CAR has remained elusive
6
. Here we describe an approach to CAR engineering in which we replace traditional CD3ζ domains with intracellular proximal T cell signalling molecules. We show that certain proximal signalling CARs, such as a ZAP-70 CAR, can activate T cells and eradicate tumours in vivo while bypassing upstream signalling proteins, including CD3ζ. The primary role of ZAP-70 is to phosphorylate LAT and SLP-76, which form a scaffold for signal propagation. We exploited the cooperative role of LAT and SLP-76 to engineer logic-gated intracellular network (LINK) CAR, a rapid and reversible Boolean-logic AND-gated CAR T cell platform that outperforms other systems in both efficacy and prevention of on-target, off-tumour toxicity. LINK CAR will expand the range of molecules that can be targeted with CAR T cells, and will enable these powerful therapeutic agents to be used for solid tumours and diverse diseases such as autoimmunity
7
and fibrosis
8
. In addition, this work shows that the internal signalling machinery of cells can be repurposed into surface receptors, which could open new avenues for cellular engineering. Although chimeric antigen receptor (CAR) T cells have altered the treatment landscape for B cell malignancies, the risk of on-target, off-tumour toxicity has hampered their development for solid tumours because most target antigens are shared with normal cells . Researchers have attempted to apply Boolean-logic gating to CAR T cells to prevent toxicity ; however, a truly safe and effective logic-gated CAR has remained elusive . Here we describe an approach to CAR engineering in which we replace traditional CD3ζ domains with intracellular proximal T cell signalling molecules. We show that certain proximal signalling CARs, such as a ZAP-70 CAR, can activate T cells and eradicate tumours in vivo while bypassing upstream signalling proteins, including CD3ζ. The primary role of ZAP-70 is to phosphorylate LAT and SLP-76, which form a scaffold for signal propagation. We exploited the cooperative role of LAT and SLP-76 to engineer logic-gated intracellular network (LINK) CAR, a rapid and reversible Boolean-logic AND-gated CAR T cell platform that outperforms other systems in both efficacy and prevention of on-target, off-tumour toxicity. LINK CAR will expand the range of molecules that can be targeted with CAR T cells, and will enable these powerful therapeutic agents to be used for solid tumours and diverse diseases such as autoimmunity and fibrosis . In addition, this work shows that the internal signalling machinery of cells can be repurposed into surface receptors, which could open new avenues for cellular engineering. Although chimeric antigen receptor (CAR) T cells have altered the treatment landscape for B cell malignancies, the risk of on-target, off-tumour toxicity has hampered their development for solid tumours because most target antigens are shared with normal cells 1 , 2 . Researchers have attempted to apply Boolean-logic gating to CAR T cells to prevent toxicity 3 – 5 ; however, a truly safe and effective logic-gated CAR has remained elusive 6 . Here we describe an approach to CAR engineering in which we replace traditional CD3ζ domains with intracellular proximal T cell signalling molecules. We show that certain proximal signalling CARs, such as a ZAP-70 CAR, can activate T cells and eradicate tumours in vivo while bypassing upstream signalling proteins, including CD3ζ. The primary role of ZAP-70 is to phosphorylate LAT and SLP-76, which form a scaffold for signal propagation. We exploited the cooperative role of LAT and SLP-76 to engineer logic-gated intracellular network (LINK) CAR, a rapid and reversible Boolean-logic AND-gated CAR T cell platform that outperforms other systems in both efficacy and prevention of on-target, off-tumour toxicity. LINK CAR will expand the range of molecules that can be targeted with CAR T cells, and will enable these powerful therapeutic agents to be used for solid tumours and diverse diseases such as autoimmunity 7 and fibrosis 8 . In addition, this work shows that the internal signalling machinery of cells can be repurposed into surface receptors, which could open new avenues for cellular engineering. Logic gating is used to develop a CAR T cell platform that is highly specific and allows the activity of T cells to be restricted to the encounter of two antigens, thus reducing on-target, off-tumour toxicity. Although chimeric antigen receptor (CAR) T cells have altered the treatment landscape for B cell malignancies, the risk of on-target, off-tumour toxicity has hampered their development for solid tumours because most target antigens are shared with normal cells1,2. Researchers have attempted to apply Boolean-logic gating to CAR T cells to prevent toxicity3-5; however, a truly safe and effective logic-gated CAR has remained elusive6. Here we describe an approach to CAR engineering in which we replace traditional CD3ζ domains with intracellular proximal T cell signalling molecules. We show that certain proximal signalling CARs, such as a ZAP-70 CAR, can activate T cells and eradicate tumours in vivo while bypassing upstream signalling proteins, including CD3ζ. The primary role of ZAP-70 is to phosphorylate LAT and SLP-76, which form a scaffold for signal propagation. We exploited the cooperative role of LAT and SLP-76 to engineer logic-gated intracellular network (LINK) CAR, a rapid and reversible Boolean-logic AND-gated CAR T cell platform that outperforms other systems in both efficacy and prevention of on-target, off-tumour toxicity. LINK CAR will expand the range of molecules that can be targeted with CAR T cells, and will enable these powerful therapeutic agents to be used for solid tumours and diverse diseases such as autoimmunity7 and fibrosis8. In addition, this work shows that the internal signalling machinery of cells can be repurposed into surface receptors, which could open new avenues for cellular engineering.Although chimeric antigen receptor (CAR) T cells have altered the treatment landscape for B cell malignancies, the risk of on-target, off-tumour toxicity has hampered their development for solid tumours because most target antigens are shared with normal cells1,2. Researchers have attempted to apply Boolean-logic gating to CAR T cells to prevent toxicity3-5; however, a truly safe and effective logic-gated CAR has remained elusive6. Here we describe an approach to CAR engineering in which we replace traditional CD3ζ domains with intracellular proximal T cell signalling molecules. We show that certain proximal signalling CARs, such as a ZAP-70 CAR, can activate T cells and eradicate tumours in vivo while bypassing upstream signalling proteins, including CD3ζ. The primary role of ZAP-70 is to phosphorylate LAT and SLP-76, which form a scaffold for signal propagation. We exploited the cooperative role of LAT and SLP-76 to engineer logic-gated intracellular network (LINK) CAR, a rapid and reversible Boolean-logic AND-gated CAR T cell platform that outperforms other systems in both efficacy and prevention of on-target, off-tumour toxicity. LINK CAR will expand the range of molecules that can be targeted with CAR T cells, and will enable these powerful therapeutic agents to be used for solid tumours and diverse diseases such as autoimmunity7 and fibrosis8. In addition, this work shows that the internal signalling machinery of cells can be repurposed into surface receptors, which could open new avenues for cellular engineering. Although chimeric antigen receptor (CAR) T cells have altered the treatment landscape for B cell malignancies, the risk of on-target, off-tumour toxicity has hampered their development for solid tumours because most target antigens are shared with normal cells1,2. Researchers have attempted to apply Boolean-logic gating to CAR T cells to prevent toxicity3-5; however, a truly safe and effective logic-gated CAR has remained elusive6. Here we describe an approach to CAR engineering in which we replace traditional CD3Z domains with intracellular proximal T cell signalling molecules. We show that certain proximal signalling CARs, such as a ZAP-70 CAR, can activate T cells and eradicate tumours in vivo while bypassing upstream signalling proteins, including CD3ζ. The primary role of ZAP-70 is to phosphorylate LAT and SLP-76, which form a scaffold for signal propagation. We exploited the cooperative role of LAT and SLP-76 to engineer logic-gated intracellular network (LINK) CAR, a rapid and reversible Boolean-logic AND-gated CAR T cell platform that outperforms other systems in both efficacy and prevention of on-target, off-tumour toxicity. LINK CAR will expand the range of molecules that can be targeted with CAR T cells, and will enable these powerful therapeutic agents to be used for solid tumours and diverse diseases such as autoimmunity7 and fibrosis8. In addition, this work shows that the internal signalling machinery of cells can be repurposed into surface receptors, which could open new avenues for cellular engineering. |
| Author | Xu, Peng Tousley, Aidan M. de la Serna, Eva L. Labanieh, Louai Kim, Won-Ju Dalton, Guillermo Nicolas Rotiroti, Maria Caterina Majzner, Robbie G. Rysavy, Lea Wenting Yin, Yajie Lareau, Caleb Sotillo, Elena Satpathy, Ansuman T. Mackall, Crystal L. Klysz, Dorota Rietberg, Skyler P. Weber, Evan W. Dunn, Alexander R. |
| AuthorAffiliation | 1 Department of Pediatrics, Stanford University School of Medicine, Stanford, CA, USA 4 Department of Pathology, Stanford University School of Medicine, Stanford, CA, USA 2 Department of Bioengineering, Stanford University, Stanford, CA, USA 10 Department of Medicine, Stanford University School of Medicine, Stanford, CA, USA 8 Stanford Cardiovascular Institute, Stanford University School of Medicine, Stanford, CA, USA 6 Department of Pediatrics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA 7 Department of Chemical Engineering, Stanford University, Stanford, CA, USA 3 Parker Institute for Cancer Immunotherapy, San Francisco, CA, USA 5 Stanford Cancer Institute, Stanford University School of Medicine, Stanford, CA, USA 9 Biophysics Program, Stanford University, Stanford, CA, USA |
| AuthorAffiliation_xml | – name: 6 Department of Pediatrics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA – name: 1 Department of Pediatrics, Stanford University School of Medicine, Stanford, CA, USA – name: 5 Stanford Cancer Institute, Stanford University School of Medicine, Stanford, CA, USA – name: 9 Biophysics Program, Stanford University, Stanford, CA, USA – name: 10 Department of Medicine, Stanford University School of Medicine, Stanford, CA, USA – name: 7 Department of Chemical Engineering, Stanford University, Stanford, CA, USA – name: 2 Department of Bioengineering, Stanford University, Stanford, CA, USA – name: 8 Stanford Cardiovascular Institute, Stanford University School of Medicine, Stanford, CA, USA – name: 3 Parker Institute for Cancer Immunotherapy, San Francisco, CA, USA – name: 4 Department of Pathology, Stanford University School of Medicine, Stanford, CA, USA |
| Author_xml | – sequence: 1 givenname: Aidan M. orcidid: 0000-0002-3286-0238 surname: Tousley fullname: Tousley, Aidan M. organization: Department of Pediatrics, Stanford University School of Medicine – sequence: 2 givenname: Maria Caterina surname: Rotiroti fullname: Rotiroti, Maria Caterina organization: Department of Pediatrics, Stanford University School of Medicine – sequence: 3 givenname: Louai surname: Labanieh fullname: Labanieh, Louai organization: Department of Bioengineering, Stanford University, Parker Institute for Cancer Immunotherapy – sequence: 4 givenname: Lea Wenting surname: Rysavy fullname: Rysavy, Lea Wenting organization: Department of Pediatrics, Stanford University School of Medicine – sequence: 5 givenname: Won-Ju orcidid: 0000-0002-1800-0485 surname: Kim fullname: Kim, Won-Ju organization: Department of Pediatrics, Stanford University School of Medicine – sequence: 6 givenname: Caleb orcidid: 0000-0003-4179-4807 surname: Lareau fullname: Lareau, Caleb organization: Parker Institute for Cancer Immunotherapy, Department of Pathology, Stanford University School of Medicine, Stanford Cancer Institute, Stanford University School of Medicine – sequence: 7 givenname: Elena orcidid: 0000-0002-3993-1932 surname: Sotillo fullname: Sotillo, Elena organization: Stanford Cancer Institute, Stanford University School of Medicine – sequence: 8 givenname: Evan W. surname: Weber fullname: Weber, Evan W. organization: Parker Institute for Cancer Immunotherapy, Department of Pediatrics, Perelman School of Medicine, University of Pennsylvania – sequence: 9 givenname: Skyler P. surname: Rietberg fullname: Rietberg, Skyler P. organization: Stanford Cancer Institute, Stanford University School of Medicine – sequence: 10 givenname: Guillermo Nicolas surname: Dalton fullname: Dalton, Guillermo Nicolas organization: Department of Pediatrics, Stanford University School of Medicine – sequence: 11 givenname: Yajie orcidid: 0000-0002-2220-005X surname: Yin fullname: Yin, Yajie organization: Parker Institute for Cancer Immunotherapy, Department of Pathology, Stanford University School of Medicine, Stanford Cancer Institute, Stanford University School of Medicine – sequence: 12 givenname: Dorota surname: Klysz fullname: Klysz, Dorota organization: Stanford Cancer Institute, Stanford University School of Medicine – sequence: 13 givenname: Peng surname: Xu fullname: Xu, Peng organization: Stanford Cancer Institute, Stanford University School of Medicine – sequence: 14 givenname: Eva L. surname: de la Serna fullname: de la Serna, Eva L. organization: Department of Chemical Engineering, Stanford University – sequence: 15 givenname: Alexander R. orcidid: 0000-0001-6096-4600 surname: Dunn fullname: Dunn, Alexander R. organization: Department of Chemical Engineering, Stanford University, Stanford Cardiovascular Institute, Stanford University School of Medicine, Biophysics Program, Stanford University – sequence: 16 givenname: Ansuman T. orcidid: 0000-0002-5167-537X surname: Satpathy fullname: Satpathy, Ansuman T. organization: Parker Institute for Cancer Immunotherapy, Department of Pathology, Stanford University School of Medicine, Stanford Cancer Institute, Stanford University School of Medicine – sequence: 17 givenname: Crystal L. orcidid: 0000-0001-6323-4304 surname: Mackall fullname: Mackall, Crystal L. organization: Department of Pediatrics, Stanford University School of Medicine, Parker Institute for Cancer Immunotherapy, Stanford Cancer Institute, Stanford University School of Medicine, Department of Medicine, Stanford University School of Medicine – sequence: 18 givenname: Robbie G. orcidid: 0000-0001-6969-8011 surname: Majzner fullname: Majzner, Robbie G. email: rmajzner@stanford.edu organization: Department of Pediatrics, Stanford University School of Medicine, Parker Institute for Cancer Immunotherapy, Stanford Cancer Institute, Stanford University School of Medicine |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/36890224$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | The Author(s), under exclusive licence to Springer Nature Limited 2023. Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law. 2023. The Author(s), under exclusive licence to Springer Nature Limited. Copyright Nature Publishing Group Mar 16, 2023 |
| Copyright_xml | – notice: The Author(s), under exclusive licence to Springer Nature Limited 2023. Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law. – notice: 2023. The Author(s), under exclusive licence to Springer Nature Limited. – notice: Copyright Nature Publishing Group Mar 16, 2023 |
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| DOI | 10.1038/s41586-023-05778-2 |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Author contributions A.M.T. conceptualized the work, cloned constructs, designed and performed experiments, analysed data and wrote the manuscript. M.C.R. conceptualized the work, designed and performed experiments and analysed data. L.L. conceptualized the work, cloned constructs and designed experiments. L.W.R. cloned constructs, performed experiments and analysed data. W.-J.K. designed and performed experiments and analysed data. C.L. and Y.Y. performed and analysed scRNA-seq experiments. E.S. designed experiments and performed molecular analyses. E.W.W. designed experiments and analysed scRNA-seq data. S.P.R. cloned constructs, designed and performed experiments and analysed data. G.N.D. performed in vivo experiments. D.K. designed experiments. P.X. performed in vivo experiments. E.L.d.l.S. performed experiments. A.T.S., C.L.M. and A.R.D. supervised and/or funded some elements of the work. R.G.M. conceptualized, funded and supervised the work, designed experiments and wrote the manuscript. All authors contributed to the editing of the manuscript. |
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| Title | Co-opting signalling molecules enables logic-gated control of CAR T cells |
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