Chimeric antigen receptor-induced antigen loss protects CD5.CART cells from fratricide without compromising on-target cytotoxicity

Chimeric antigen receptor T cells (CART) targeting lymphocyte antigens can induce T cell fratricide and require additional engineering to mitigate self-damage. We demonstrate that the expression of a chimeric antigen receptor (CAR) targeting CD5, a prominent pan-T cell antigen, induces rapid interna...

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Published inCell reports. Medicine Vol. 5; no. 7; p. 101628
Main Authors Ma, Royce, Woods, Mae, Burkhardt, Phillip, Crooks, Noah, van Leeuwen, Dayenne G., Shmidt, Daniil, Couturier, Jacob, Chaumette, Alexandre, Popat, Divya, Hill, LaQuisa C., Rouce, Rayne H., Thakkar, Sachin, Orozco, Aaron F., Carisey, Alexandre F., Brenner, Malcolm K., Mamonkin, Maksim
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 16.07.2024
Elsevier
Subjects
Animals
CAR
CD5
CD5 Antigens - metabolism
chimeric antigen receptor
clinical trials
Cytotoxicity, Immunologic
fratricide
Humans
Immunotherapy, Adoptive - methods
off-tumor toxicity
Receptors, Antigen, T-Cell - immunology
Receptors, Antigen, T-Cell - metabolism
Receptors, Chimeric Antigen - immunology
Receptors, Chimeric Antigen - metabolism
T cell fratricide
T cell malignancies
T-Lymphocytes - immunology
T-Lymphocytes - metabolism
off-tumor toxicity
CD5
CAR
chimeric antigen receptor
clinical trials
T cell fratricide
T cell malignancies
fratricide
Online AccessGet full text

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Abstract Chimeric antigen receptor T cells (CART) targeting lymphocyte antigens can induce T cell fratricide and require additional engineering to mitigate self-damage. We demonstrate that the expression of a chimeric antigen receptor (CAR) targeting CD5, a prominent pan-T cell antigen, induces rapid internalization and complete loss of the CD5 protein on T cells, protecting them from self-targeting. Notably, exposure of healthy and malignant T cells to CD5.CART cells induces similar internalization of CD5 on target cells, transiently shielding them from cytotoxicity. However, this protection is short-lived, as sustained activity of CD5.CART cells in patients with T cell malignancies results in full ablation of CD5+ T cells while sparing healthy T cells naturally lacking CD5. These results indicate that continuous downmodulation of the target antigen in CD5.CART cells produces effective fratricide resistance without undermining their on-target cytotoxicity. [Display omitted] •CD5 is highly expressed in T cell malignancies and normal T cells•CD5.CAR causes full degradation of CD5 in T cells leading to fratricide resistance•CD5.CAR transiently downmodulates CD5 on target cells in trans•CD5 modulation in trans does not protect target cells from CD5.CART cells long-term CD5 is a pan-T cell marker highly expressed in T cell cancers. Ma et al. show that expression of CD5.CAR in T cells drives full degradation of CD5 to achieve fratricide resistance. While CD5.CAR also transiently downmodulates CD5 in trans on target T cells, this process does not protect them from elimination long term.
AbstractList Chimeric antigen receptor T cells (CART) targeting lymphocyte antigens can induce T cell fratricide and require additional engineering to mitigate self-damage. We demonstrate that the expression of a chimeric antigen receptor (CAR) targeting CD5, a prominent pan-T cell antigen, induces rapid internalization and complete loss of the CD5 protein on T cells, protecting them from self-targeting. Notably, exposure of healthy and malignant T cells to CD5.CART cells induces similar internalization of CD5 on target cells, transiently shielding them from cytotoxicity. However, this protection is short-lived, as sustained activity of CD5.CART cells in patients with T cell malignancies results in full ablation of CD5 + T cells while sparing healthy T cells naturally lacking CD5. These results indicate that continuous downmodulation of the target antigen in CD5.CART cells produces effective fratricide resistance without undermining their on-target cytotoxicity. • CD5 is highly expressed in T cell malignancies and normal T cells • CD5.CAR causes full degradation of CD5 in T cells leading to fratricide resistance • CD5.CAR transiently downmodulates CD5 on target cells in trans • CD5 modulation in trans does not protect target cells from CD5.CART cells long-term CD5 is a pan-T cell marker highly expressed in T cell cancers. Ma et al. show that expression of CD5.CAR in T cells drives full degradation of CD5 to achieve fratricide resistance. While CD5.CAR also transiently downmodulates CD5 in trans on target T cells, this process does not protect them from elimination long term.
Chimeric antigen receptor T cells (CART) targeting lymphocyte antigens can induce T cell fratricide and require additional engineering to mitigate self-damage. We demonstrate that the expression of a chimeric antigen receptor (CAR) targeting CD5, a prominent pan-T cell antigen, induces rapid internalization and complete loss of the CD5 protein on T cells, protecting them from self-targeting. Notably, exposure of healthy and malignant T cells to CD5.CART cells induces similar internalization of CD5 on target cells, transiently shielding them from cytotoxicity. However, this protection is short-lived, as sustained activity of CD5.CART cells in patients with T cell malignancies results in full ablation of CD5+ T cells while sparing healthy T cells naturally lacking CD5. These results indicate that continuous downmodulation of the target antigen in CD5.CART cells produces effective fratricide resistance without undermining their on-target cytotoxicity.Chimeric antigen receptor T cells (CART) targeting lymphocyte antigens can induce T cell fratricide and require additional engineering to mitigate self-damage. We demonstrate that the expression of a chimeric antigen receptor (CAR) targeting CD5, a prominent pan-T cell antigen, induces rapid internalization and complete loss of the CD5 protein on T cells, protecting them from self-targeting. Notably, exposure of healthy and malignant T cells to CD5.CART cells induces similar internalization of CD5 on target cells, transiently shielding them from cytotoxicity. However, this protection is short-lived, as sustained activity of CD5.CART cells in patients with T cell malignancies results in full ablation of CD5+ T cells while sparing healthy T cells naturally lacking CD5. These results indicate that continuous downmodulation of the target antigen in CD5.CART cells produces effective fratricide resistance without undermining their on-target cytotoxicity.
Chimeric antigen receptor T cells (CART) targeting lymphocyte antigens can induce T cell fratricide and require additional engineering to mitigate self-damage. We demonstrate that the expression of a chimeric antigen receptor (CAR) targeting CD5, a prominent pan-T cell antigen, induces rapid internalization and complete loss of the CD5 protein on T cells, protecting them from self-targeting. Notably, exposure of healthy and malignant T cells to CD5.CART cells induces similar internalization of CD5 on target cells, transiently shielding them from cytotoxicity. However, this protection is short-lived, as sustained activity of CD5.CART cells in patients with T cell malignancies results in full ablation of CD5 T cells while sparing healthy T cells naturally lacking CD5. These results indicate that continuous downmodulation of the target antigen in CD5.CART cells produces effective fratricide resistance without undermining their on-target cytotoxicity.
Chimeric antigen receptor T cells (CART) targeting lymphocyte antigens can induce T cell fratricide and require additional engineering to mitigate self-damage. We demonstrate that the expression of a chimeric antigen receptor (CAR) targeting CD5, a prominent pan-T cell antigen, induces rapid internalization and complete loss of the CD5 protein on T cells, protecting them from self-targeting. Notably, exposure of healthy and malignant T cells to CD5.CART cells induces similar internalization of CD5 on target cells, transiently shielding them from cytotoxicity. However, this protection is short-lived, as sustained activity of CD5.CART cells in patients with T cell malignancies results in full ablation of CD5+ T cells while sparing healthy T cells naturally lacking CD5. These results indicate that continuous downmodulation of the target antigen in CD5.CART cells produces effective fratricide resistance without undermining their on-target cytotoxicity. [Display omitted] •CD5 is highly expressed in T cell malignancies and normal T cells•CD5.CAR causes full degradation of CD5 in T cells leading to fratricide resistance•CD5.CAR transiently downmodulates CD5 on target cells in trans•CD5 modulation in trans does not protect target cells from CD5.CART cells long-term CD5 is a pan-T cell marker highly expressed in T cell cancers. Ma et al. show that expression of CD5.CAR in T cells drives full degradation of CD5 to achieve fratricide resistance. While CD5.CAR also transiently downmodulates CD5 in trans on target T cells, this process does not protect them from elimination long term.
ArticleNumber 101628
Author Popat, Divya
Brenner, Malcolm K.
Shmidt, Daniil
van Leeuwen, Dayenne G.
Burkhardt, Phillip
Thakkar, Sachin
Rouce, Rayne H.
Crooks, Noah
Mamonkin, Maksim
Ma, Royce
Couturier, Jacob
Chaumette, Alexandre
Woods, Mae
Orozco, Aaron F.
Carisey, Alexandre F.
Hill, LaQuisa C.
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Keywords off-tumor toxicity
CD5
CAR
chimeric antigen receptor
clinical trials
T cell fratricide
T cell malignancies
fratricide
Language English
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SSID ssj0002511830
Score 2.3175404
Snippet Chimeric antigen receptor T cells (CART) targeting lymphocyte antigens can induce T cell fratricide and require additional engineering to mitigate self-damage....
Chimeric antigen receptor T cells (CART) targeting lymphocyte antigens can induce T cell fratricide and require additional engineering to mitigate self-damage....
SourceID pubmedcentral
proquest
crossref
pubmed
elsevier
SourceType Open Access Repository
Aggregation Database
Index Database
Publisher
StartPage 101628
SubjectTerms Animals
CAR
CD5
CD5 Antigens - metabolism
chimeric antigen receptor
clinical trials
Cytotoxicity, Immunologic
fratricide
Humans
Immunotherapy, Adoptive - methods
off-tumor toxicity
Receptors, Antigen, T-Cell - immunology
Receptors, Antigen, T-Cell - metabolism
Receptors, Chimeric Antigen - immunology
Receptors, Chimeric Antigen - metabolism
T cell fratricide
T cell malignancies
T-Lymphocytes - immunology
T-Lymphocytes - metabolism
Title Chimeric antigen receptor-induced antigen loss protects CD5.CART cells from fratricide without compromising on-target cytotoxicity
URI https://dx.doi.org/10.1016/j.xcrm.2024.101628
https://www.ncbi.nlm.nih.gov/pubmed/38986621
https://www.proquest.com/docview/3078714947
https://pubmed.ncbi.nlm.nih.gov/PMC11293353
Volume 5
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