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         headline:TIGIT is the central player in T-cell suppression associated with CAR T-cell relapse in mantle cell lymphoma
         description:Chimeric antigen receptor (CAR) T-cell therapy using brexucabtagene autoleucel (BA) induces remission in many patients with mantle cell lymphoma (MCL), and BA is the only CAR T-cell therapy approved by the FDA for MCL. However, development of relapses to BA is recognized with poor patient outcomes. Multiple CAR T-cell therapies have been approved for other lymphomas and the resistance mechanisms have been investigated. However, the mechanisms underlying BA relapse in MCL have not been investigated and whether any previously reported resistance mechanisms apply to BA-relapsed patients with MCL is unknown. To interrogate BA resistance mechanisms in MCL, we performed single-cell RNA sequencing on 39 longitudinally collected samples from 15 BA-treated patients, and multiplex cytokine profiling on 80 serial samples from 20 patients. We demonstrate that after BA relapse, the proportion of T cells, especially cytotoxic T cells (CTLs), decreased among non-tumor cells, while the proportion of myeloid cells correspondingly increased. TIGIT, LAG3, and CD96 were the predominant checkpoint molecules expressed on exhausted T cells and CTLs; only TIGIT was significantly increased after relapse. CTLs expanded during remission, and then contracted during relapse with upregulated TIGIT expression. Tumor cells also acquired TIGIT expression after relapse, leading to the enhanced interaction of tumor cell TIGIT with monocyte CD155/PVR. In myeloid cells, post-relapse HLA-II expression was reduced relative to pretreatment and during remission. Myeloid-derived suppressor cells (MDSCs) were enriched after relapse with elevated expression of activation markers, including CLU (clusterin) and VCAN (versican). Extracellular chemokines (CCL4, CXCL9, CXCL13), soluble checkpoint inhibitors (sPD-L1, sTIM3, s4-1BB), and soluble receptors (sIL-2R, sTNFRII) were decreased during remission but elevated after relapse. Our data demonstrate that multiple tumor-intrinsic and -extrinsic factors are associated with T-cell suppression and BA relapse. Among these, TIGIT appears to be the central player given its elevated expression after BA relapse in not only CTLs but also MCL cells. The acquisition of TIGIT expression on tumor cells is MCL-specific and has not been reported in other CAR T-treated diseases. Together, our data suggest that co-targeting TIGIT may prevent CAR T relapses and thus promote long-term progression-free survival in MCL patients.
         datePublished:2022-09-26T00:00:00Z
         dateModified:2022-09-26T00:00:00Z
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            Mantle cell lymphoma
            CAR T-cell therapy
            Relapse
            T cell suppression
            Myeloid-derived suppressor cells
            Immune checkpoint
            TIGIT
            Cytokines
            Chemokines
            Soluble receptors
            Cancer Research
            Oncology
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      headline:TIGIT is the central player in T-cell suppression associated with CAR T-cell relapse in mantle cell lymphoma
      description:Chimeric antigen receptor (CAR) T-cell therapy using brexucabtagene autoleucel (BA) induces remission in many patients with mantle cell lymphoma (MCL), and BA is the only CAR T-cell therapy approved by the FDA for MCL. However, development of relapses to BA is recognized with poor patient outcomes. Multiple CAR T-cell therapies have been approved for other lymphomas and the resistance mechanisms have been investigated. However, the mechanisms underlying BA relapse in MCL have not been investigated and whether any previously reported resistance mechanisms apply to BA-relapsed patients with MCL is unknown. To interrogate BA resistance mechanisms in MCL, we performed single-cell RNA sequencing on 39 longitudinally collected samples from 15 BA-treated patients, and multiplex cytokine profiling on 80 serial samples from 20 patients. We demonstrate that after BA relapse, the proportion of T cells, especially cytotoxic T cells (CTLs), decreased among non-tumor cells, while the proportion of myeloid cells correspondingly increased. TIGIT, LAG3, and CD96 were the predominant checkpoint molecules expressed on exhausted T cells and CTLs; only TIGIT was significantly increased after relapse. CTLs expanded during remission, and then contracted during relapse with upregulated TIGIT expression. Tumor cells also acquired TIGIT expression after relapse, leading to the enhanced interaction of tumor cell TIGIT with monocyte CD155/PVR. In myeloid cells, post-relapse HLA-II expression was reduced relative to pretreatment and during remission. Myeloid-derived suppressor cells (MDSCs) were enriched after relapse with elevated expression of activation markers, including CLU (clusterin) and VCAN (versican). Extracellular chemokines (CCL4, CXCL9, CXCL13), soluble checkpoint inhibitors (sPD-L1, sTIM3, s4-1BB), and soluble receptors (sIL-2R, sTNFRII) were decreased during remission but elevated after relapse. Our data demonstrate that multiple tumor-intrinsic and -extrinsic factors are associated with T-cell suppression and BA relapse. Among these, TIGIT appears to be the central player given its elevated expression after BA relapse in not only CTLs but also MCL cells. The acquisition of TIGIT expression on tumor cells is MCL-specific and has not been reported in other CAR T-treated diseases. Together, our data suggest that co-targeting TIGIT may prevent CAR T relapses and thus promote long-term progression-free survival in MCL patients.
      datePublished:2022-09-26T00:00:00Z
      dateModified:2022-09-26T00:00:00Z
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      pageEnd:16
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      sameAs:https://doi.org/10.1186/s12943-022-01655-0
      keywords:
         Mantle cell lymphoma
         CAR T-cell therapy
         Relapse
         T cell suppression
         Myeloid-derived suppressor cells
         Immune checkpoint
         TIGIT
         Cytokines
         Chemokines
         Soluble receptors
         Cancer Research
         Oncology
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            name:Vivian Changying Jiang
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            name:Dapeng Hao
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         name:Department of Lymphoma and Myeloma, the University of Texas MD Anderson Cancer Center, Houston, USA
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         name:Department of Lymphoma and Myeloma, the University of Texas MD Anderson Cancer Center, Houston, USA
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         name:Department of Lymphoma and Myeloma, the University of Texas MD Anderson Cancer Center, Houston, USA
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         name:Department of Lymphoma and Myeloma, the University of Texas MD Anderson Cancer Center, Houston, USA
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      address:
         name:Department of Genomic Medicine, the University of Texas MD Anderson Cancer Center, Houston, USA
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      address:
         name:Department of Genomic Medicine, the University of Texas MD Anderson Cancer Center, Houston, USA
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         name:Department of Genomic Medicine, the University of Texas MD Anderson Cancer Center, Houston, USA
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         name:Department of Genomic Medicine, the University of Texas MD Anderson Cancer Center, Houston, USA
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         name:Department of Genomic Medicine, the University of Texas MD Anderson Cancer Center, Houston, USA
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      name:Vivian Changying Jiang
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            name:the University of Texas MD Anderson Cancer Center
            address:
               name:Department of Lymphoma and Myeloma, the University of Texas MD Anderson Cancer Center, Houston, USA
               type:PostalAddress
            type:Organization
      name:Dapeng Hao
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            address:
               name:Department of Genomic Medicine, the University of Texas MD Anderson Cancer Center, Houston, USA
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      name:Preetesh Jain
      affiliation:
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            address:
               name:Department of Lymphoma and Myeloma, the University of Texas MD Anderson Cancer Center, Houston, USA
               type:PostalAddress
            type:Organization
      name:Yijing Li
      affiliation:
            name:the University of Texas MD Anderson Cancer Center
            address:
               name:Department of Lymphoma and Myeloma, the University of Texas MD Anderson Cancer Center, Houston, USA
               type:PostalAddress
            type:Organization
      name:Qingsong Cai
      affiliation:
            name:the University of Texas MD Anderson Cancer Center
            address:
               name:Department of Lymphoma and Myeloma, the University of Texas MD Anderson Cancer Center, Houston, USA
               type:PostalAddress
            type:Organization
      name:Yixin Yao
      affiliation:
            name:the University of Texas MD Anderson Cancer Center
            address:
               name:Department of Lymphoma and Myeloma, the University of Texas MD Anderson Cancer Center, Houston, USA
               type:PostalAddress
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      name:Lei Nie
      affiliation:
            name:the University of Texas MD Anderson Cancer Center
            address:
               name:Department of Lymphoma and Myeloma, the University of Texas MD Anderson Cancer Center, Houston, USA
               type:PostalAddress
            type:Organization
      name:Yang Liu
      affiliation:
            name:the University of Texas MD Anderson Cancer Center
            address:
               name:Department of Lymphoma and Myeloma, the University of Texas MD Anderson Cancer Center, Houston, USA
               type:PostalAddress
            type:Organization
      name:Jingling Jin
      affiliation:
            name:the University of Texas MD Anderson Cancer Center
            address:
               name:Department of Lymphoma and Myeloma, the University of Texas MD Anderson Cancer Center, Houston, USA
               type:PostalAddress
            type:Organization
      name:Wei Wang
      affiliation:
            name:the University of Texas MD Anderson Cancer Center
            address:
               name:Department of Lymphoma and Myeloma, the University of Texas MD Anderson Cancer Center, Houston, USA
               type:PostalAddress
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      name:Heng-Huan Lee
      affiliation:
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            address:
               name:Department of Lymphoma and Myeloma, the University of Texas MD Anderson Cancer Center, Houston, USA
               type:PostalAddress
            type:Organization
      name:Yuxuan Che
      affiliation:
            name:the University of Texas MD Anderson Cancer Center
            address:
               name:Department of Lymphoma and Myeloma, the University of Texas MD Anderson Cancer Center, Houston, USA
               type:PostalAddress
            type:Organization
      name:Enyu Dai
      affiliation:
            name:the University of Texas MD Anderson Cancer Center
            address:
               name:Department of Genomic Medicine, the University of Texas MD Anderson Cancer Center, Houston, USA
               type:PostalAddress
            type:Organization
      name:Guangchun Han
      affiliation:
            name:the University of Texas MD Anderson Cancer Center
            address:
               name:Department of Genomic Medicine, the University of Texas MD Anderson Cancer Center, Houston, USA
               type:PostalAddress
            type:Organization
      name:Ruiping Wang
      affiliation:
            name:the University of Texas MD Anderson Cancer Center
            address:
               name:Department of Genomic Medicine, the University of Texas MD Anderson Cancer Center, Houston, USA
               type:PostalAddress
            type:Organization
      name:Kunal Rai
      affiliation:
            name:the University of Texas MD Anderson Cancer Center
            address:
               name:Department of Genomic Medicine, the University of Texas MD Anderson Cancer Center, Houston, USA
               type:PostalAddress
            type:Organization
      name:Andrew Futreal
      affiliation:
            name:the University of Texas MD Anderson Cancer Center
            address:
               name:Department of Genomic Medicine, the University of Texas MD Anderson Cancer Center, Houston, USA
               type:PostalAddress
            type:Organization
      name:Christopher Flowers
      affiliation:
            name:the University of Texas MD Anderson Cancer Center
            address:
               name:Department of Lymphoma and Myeloma, the University of Texas MD Anderson Cancer Center, Houston, USA
               type:PostalAddress
            type:Organization
      name:Linghua Wang
      affiliation:
            name:the University of Texas MD Anderson Cancer Center
            address:
               name:Department of Genomic Medicine, the University of Texas MD Anderson Cancer Center, Houston, USA
               type:PostalAddress
            type:Organization
            name:The University of Texas MD Anderson Cancer Center UTHealth Graduate School of Biomedical Sciences (GSBS)
            address:
               name:The University of Texas MD Anderson Cancer Center UTHealth Graduate School of Biomedical Sciences (GSBS), Houston, USA
               type:PostalAddress
            type:Organization
      email:[email protected]
      name:Michael Wang
      affiliation:
            name:the University of Texas MD Anderson Cancer Center
            address:
               name:Department of Lymphoma and Myeloma, the University of Texas MD Anderson Cancer Center, Houston, USA
               type:PostalAddress
            type:Organization
            name:the University of Texas MD Anderson Cancer Center
            address:
               name:Department of Stem Cell Transplantation and Cellular Therapy, the University of Texas MD Anderson Cancer Center, Houston, USA
               type:PostalAddress
            type:Organization
      email:[email protected]
PostalAddress:
      name:Department of Lymphoma and Myeloma, the University of Texas MD Anderson Cancer Center, Houston, USA
      name:Department of Genomic Medicine, the University of Texas MD Anderson Cancer Center, Houston, USA
      name:Department of Lymphoma and Myeloma, the University of Texas MD Anderson Cancer Center, Houston, USA
      name:Department of Lymphoma and Myeloma, the University of Texas MD Anderson Cancer Center, Houston, USA
      name:Department of Lymphoma and Myeloma, the University of Texas MD Anderson Cancer Center, Houston, USA
      name:Department of Lymphoma and Myeloma, the University of Texas MD Anderson Cancer Center, Houston, USA
      name:Department of Lymphoma and Myeloma, the University of Texas MD Anderson Cancer Center, Houston, USA
      name:Department of Lymphoma and Myeloma, the University of Texas MD Anderson Cancer Center, Houston, USA
      name:Department of Lymphoma and Myeloma, the University of Texas MD Anderson Cancer Center, Houston, USA
      name:Department of Lymphoma and Myeloma, the University of Texas MD Anderson Cancer Center, Houston, USA
      name:Department of Lymphoma and Myeloma, the University of Texas MD Anderson Cancer Center, Houston, USA
      name:Department of Lymphoma and Myeloma, the University of Texas MD Anderson Cancer Center, Houston, USA
      name:Department of Genomic Medicine, the University of Texas MD Anderson Cancer Center, Houston, USA
      name:Department of Genomic Medicine, the University of Texas MD Anderson Cancer Center, Houston, USA
      name:Department of Genomic Medicine, the University of Texas MD Anderson Cancer Center, Houston, USA
      name:Department of Genomic Medicine, the University of Texas MD Anderson Cancer Center, Houston, USA
      name:Department of Genomic Medicine, the University of Texas MD Anderson Cancer Center, Houston, USA
      name:Department of Lymphoma and Myeloma, the University of Texas MD Anderson Cancer Center, Houston, USA
      name:Department of Genomic Medicine, the University of Texas MD Anderson Cancer Center, Houston, USA
      name:The University of Texas MD Anderson Cancer Center UTHealth Graduate School of Biomedical Sciences (GSBS), Houston, USA
      name:Department of Lymphoma and Myeloma, the University of Texas MD Anderson Cancer Center, Houston, USA
      name:Department of Stem Cell Transplantation and Cellular Therapy, the University of Texas MD Anderson Cancer Center, Houston, USA

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