Novel banana lectin CAR-T cells to target pancreatic tumors and tumor-associated stroma
BackgroundCell therapies for solid tumors are thwarted by the hostile tumor microenvironment (TME) and by heterogeneous expression of tumor target antigens. We address both limitations with a novel class of chimeric antigen receptors based on plant lectins, which recognize the aberrant sugar residue...
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| Published in | Journal for immunotherapy of cancer Vol. 11; no. 1; p. e005891 |
|---|---|
| Main Authors | , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
England
BMJ Publishing Group Ltd
01.01.2023
BMJ Publishing Group LTD BMJ Publishing Group |
| Series | Original research |
| Subjects | |
| Online Access | Get full text |
| ISSN | 2051-1426 2051-1426 |
| DOI | 10.1136/jitc-2022-005891 |
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| Abstract | BackgroundCell therapies for solid tumors are thwarted by the hostile tumor microenvironment (TME) and by heterogeneous expression of tumor target antigens. We address both limitations with a novel class of chimeric antigen receptors based on plant lectins, which recognize the aberrant sugar residues that are a ‘hallmark’ of both malignant and associated stromal cells. We have expressed in T cells a modified lectin from banana, H84T BanLec, attached to a chimeric antigen receptor (H84T-CAR) that recognizes high-mannose (asparagine residue with five to nine mannoses). Here, we tested the efficacy of our novel H84T CAR in models of pancreatic ductal adenocarcinoma (PDAC), intractable tumors with aberrant glycosylation and characterized by desmoplastic stroma largely contributed by pancreatic stellate cells (PSCs).MethodsWe transduced human T cells with a second-generation retroviral construct expressing the H84T BanLec chimeric receptor, measured T-cell expansion, characterized T-cell phenotype, and tested their efficacy against PDAC tumor cells lines by flow cytometry quantification. In three-dimensional (3D) spheroid models, we measured H84T CAR T-cell disruption of PSC architecture, and T-cell infiltration by live imaging. We tested the activity of H84T CAR T cells against tumor xenografts derived from three PDAC cell lines. Antitumor activity was quantified by caliper measurement and bioluminescence signal and used anti-human vimentin to measure residual PSCs.ResultsH84T BanLec CAR was successfully transduced and expressed by T cells which had robust expansion and retained central memory phenotype in both CD4 and CD8 compartments. H84T CAR T cells targeted and eliminated PDAC tumor cell lines. They also disrupted PSC architecture in 3D models in vitro and reduced total tumor and stroma cells in mixed co-cultures. H84T CAR T cells exhibited improved T-cell infiltration in multicellular spheroids and had potent antitumor effects in the xenograft models. We observed no adverse effects against normal tissues.ConclusionsT cells expressing H84T CAR target malignant cells and their stroma in PDAC tumor models. The incorporation of glycan-targeting lectins within CARs thus extends their activity to include both malignant cells and their supporting stromal cells, disrupting the TME that otherwise diminishes the activity of cellular therapies against solid tumors. |
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| AbstractList | Cell therapies for solid tumors are thwarted by the hostile tumor microenvironment (TME) and by heterogeneous expression of tumor target antigens. We address both limitations with a novel class of chimeric antigen receptors based on plant lectins, which recognize the aberrant sugar residues that are a 'hallmark' of both malignant and associated stromal cells. We have expressed in T cells a modified lectin from banana, H84T BanLec, attached to a chimeric antigen receptor (H84T-CAR) that recognizes high-mannose (asparagine residue with five to nine mannoses). Here, we tested the efficacy of our novel H84T CAR in models of pancreatic ductal adenocarcinoma (PDAC), intractable tumors with aberrant glycosylation and characterized by desmoplastic stroma largely contributed by pancreatic stellate cells (PSCs).
We transduced human T cells with a second-generation retroviral construct expressing the H84T BanLec chimeric receptor, measured T-cell expansion, characterized T-cell phenotype, and tested their efficacy against PDAC tumor cells lines by flow cytometry quantification. In three-dimensional (3D) spheroid models, we measured H84T CAR T-cell disruption of PSC architecture, and T-cell infiltration by live imaging. We tested the activity of H84T CAR T cells against tumor xenografts derived from three PDAC cell lines. Antitumor activity was quantified by caliper measurement and bioluminescence signal and used anti-human vimentin to measure residual PSCs.
H84T BanLec CAR was successfully transduced and expressed by T cells which had robust expansion and retained central memory phenotype in both CD4 and CD8 compartments. H84T CAR T cells targeted and eliminated PDAC tumor cell lines. They also disrupted PSC architecture in 3D models in vitro and reduced total tumor and stroma cells in mixed co-cultures. H84T CAR T cells exhibited improved T-cell infiltration in multicellular spheroids and had potent antitumor effects in the xenograft models. We observed no adverse effects against normal tissues.
T cells expressing H84T CAR target malignant cells and their stroma in PDAC tumor models. The incorporation of glycan-targeting lectins within CARs thus extends their activity to include both malignant cells and their supporting stromal cells, disrupting the TME that otherwise diminishes the activity of cellular therapies against solid tumors. Background Cell therapies for solid tumors are thwarted by the hostile tumor microenvironment (TME) and by heterogeneous expression of tumor target antigens. We address both limitations with a novel class of chimeric antigen receptors based on plant lectins, which recognize the aberrant sugar residues that are a ‘hallmark’ of both malignant and associated stromal cells. We have expressed in T cells a modified lectin from banana, H84T BanLec, attached to a chimeric antigen receptor (H84T-CAR) that recognizes high-mannose (asparagine residue with five to nine mannoses). Here, we tested the efficacy of our novel H84T CAR in models of pancreatic ductal adenocarcinoma (PDAC), intractable tumors with aberrant glycosylation and characterized by desmoplastic stroma largely contributed by pancreatic stellate cells (PSCs).Methods We transduced human T cells with a second-generation retroviral construct expressing the H84T BanLec chimeric receptor, measured T-cell expansion, characterized T-cell phenotype, and tested their efficacy against PDAC tumor cells lines by flow cytometry quantification. In three-dimensional (3D) spheroid models, we measured H84T CAR T-cell disruption of PSC architecture, and T-cell infiltration by live imaging. We tested the activity of H84T CAR T cells against tumor xenografts derived from three PDAC cell lines. Antitumor activity was quantified by caliper measurement and bioluminescence signal and used anti-human vimentin to measure residual PSCs.Results H84T BanLec CAR was successfully transduced and expressed by T cells which had robust expansion and retained central memory phenotype in both CD4 and CD8 compartments. H84T CAR T cells targeted and eliminated PDAC tumor cell lines. They also disrupted PSC architecture in 3D models in vitro and reduced total tumor and stroma cells in mixed co-cultures. H84T CAR T cells exhibited improved T-cell infiltration in multicellular spheroids and had potent antitumor effects in the xenograft models. We observed no adverse effects against normal tissues.Conclusions T cells expressing H84T CAR target malignant cells and their stroma in PDAC tumor models. The incorporation of glycan-targeting lectins within CARs thus extends their activity to include both malignant cells and their supporting stromal cells, disrupting the TME that otherwise diminishes the activity of cellular therapies against solid tumors. Cell therapies for solid tumors are thwarted by the hostile tumor microenvironment (TME) and by heterogeneous expression of tumor target antigens. We address both limitations with a novel class of chimeric antigen receptors based on plant lectins, which recognize the aberrant sugar residues that are a 'hallmark' of both malignant and associated stromal cells. We have expressed in T cells a modified lectin from banana, H84T BanLec, attached to a chimeric antigen receptor (H84T-CAR) that recognizes high-mannose (asparagine residue with five to nine mannoses). Here, we tested the efficacy of our novel H84T CAR in models of pancreatic ductal adenocarcinoma (PDAC), intractable tumors with aberrant glycosylation and characterized by desmoplastic stroma largely contributed by pancreatic stellate cells (PSCs).BACKGROUNDCell therapies for solid tumors are thwarted by the hostile tumor microenvironment (TME) and by heterogeneous expression of tumor target antigens. We address both limitations with a novel class of chimeric antigen receptors based on plant lectins, which recognize the aberrant sugar residues that are a 'hallmark' of both malignant and associated stromal cells. We have expressed in T cells a modified lectin from banana, H84T BanLec, attached to a chimeric antigen receptor (H84T-CAR) that recognizes high-mannose (asparagine residue with five to nine mannoses). Here, we tested the efficacy of our novel H84T CAR in models of pancreatic ductal adenocarcinoma (PDAC), intractable tumors with aberrant glycosylation and characterized by desmoplastic stroma largely contributed by pancreatic stellate cells (PSCs).We transduced human T cells with a second-generation retroviral construct expressing the H84T BanLec chimeric receptor, measured T-cell expansion, characterized T-cell phenotype, and tested their efficacy against PDAC tumor cells lines by flow cytometry quantification. In three-dimensional (3D) spheroid models, we measured H84T CAR T-cell disruption of PSC architecture, and T-cell infiltration by live imaging. We tested the activity of H84T CAR T cells against tumor xenografts derived from three PDAC cell lines. Antitumor activity was quantified by caliper measurement and bioluminescence signal and used anti-human vimentin to measure residual PSCs.METHODSWe transduced human T cells with a second-generation retroviral construct expressing the H84T BanLec chimeric receptor, measured T-cell expansion, characterized T-cell phenotype, and tested their efficacy against PDAC tumor cells lines by flow cytometry quantification. In three-dimensional (3D) spheroid models, we measured H84T CAR T-cell disruption of PSC architecture, and T-cell infiltration by live imaging. We tested the activity of H84T CAR T cells against tumor xenografts derived from three PDAC cell lines. Antitumor activity was quantified by caliper measurement and bioluminescence signal and used anti-human vimentin to measure residual PSCs.H84T BanLec CAR was successfully transduced and expressed by T cells which had robust expansion and retained central memory phenotype in both CD4 and CD8 compartments. H84T CAR T cells targeted and eliminated PDAC tumor cell lines. They also disrupted PSC architecture in 3D models in vitro and reduced total tumor and stroma cells in mixed co-cultures. H84T CAR T cells exhibited improved T-cell infiltration in multicellular spheroids and had potent antitumor effects in the xenograft models. We observed no adverse effects against normal tissues.RESULTSH84T BanLec CAR was successfully transduced and expressed by T cells which had robust expansion and retained central memory phenotype in both CD4 and CD8 compartments. H84T CAR T cells targeted and eliminated PDAC tumor cell lines. They also disrupted PSC architecture in 3D models in vitro and reduced total tumor and stroma cells in mixed co-cultures. H84T CAR T cells exhibited improved T-cell infiltration in multicellular spheroids and had potent antitumor effects in the xenograft models. We observed no adverse effects against normal tissues.T cells expressing H84T CAR target malignant cells and their stroma in PDAC tumor models. The incorporation of glycan-targeting lectins within CARs thus extends their activity to include both malignant cells and their supporting stromal cells, disrupting the TME that otherwise diminishes the activity of cellular therapies against solid tumors.CONCLUSIONST cells expressing H84T CAR target malignant cells and their stroma in PDAC tumor models. The incorporation of glycan-targeting lectins within CARs thus extends their activity to include both malignant cells and their supporting stromal cells, disrupting the TME that otherwise diminishes the activity of cellular therapies against solid tumors. BackgroundCell therapies for solid tumors are thwarted by the hostile tumor microenvironment (TME) and by heterogeneous expression of tumor target antigens. We address both limitations with a novel class of chimeric antigen receptors based on plant lectins, which recognize the aberrant sugar residues that are a ‘hallmark’ of both malignant and associated stromal cells. We have expressed in T cells a modified lectin from banana, H84T BanLec, attached to a chimeric antigen receptor (H84T-CAR) that recognizes high-mannose (asparagine residue with five to nine mannoses). Here, we tested the efficacy of our novel H84T CAR in models of pancreatic ductal adenocarcinoma (PDAC), intractable tumors with aberrant glycosylation and characterized by desmoplastic stroma largely contributed by pancreatic stellate cells (PSCs).MethodsWe transduced human T cells with a second-generation retroviral construct expressing the H84T BanLec chimeric receptor, measured T-cell expansion, characterized T-cell phenotype, and tested their efficacy against PDAC tumor cells lines by flow cytometry quantification. In three-dimensional (3D) spheroid models, we measured H84T CAR T-cell disruption of PSC architecture, and T-cell infiltration by live imaging. We tested the activity of H84T CAR T cells against tumor xenografts derived from three PDAC cell lines. Antitumor activity was quantified by caliper measurement and bioluminescence signal and used anti-human vimentin to measure residual PSCs.ResultsH84T BanLec CAR was successfully transduced and expressed by T cells which had robust expansion and retained central memory phenotype in both CD4 and CD8 compartments. H84T CAR T cells targeted and eliminated PDAC tumor cell lines. They also disrupted PSC architecture in 3D models in vitro and reduced total tumor and stroma cells in mixed co-cultures. H84T CAR T cells exhibited improved T-cell infiltration in multicellular spheroids and had potent antitumor effects in the xenograft models. We observed no adverse effects against normal tissues.ConclusionsT cells expressing H84T CAR target malignant cells and their stroma in PDAC tumor models. The incorporation of glycan-targeting lectins within CARs thus extends their activity to include both malignant cells and their supporting stromal cells, disrupting the TME that otherwise diminishes the activity of cellular therapies against solid tumors. |
| Author | McKenna, Mary K Legendre, Maureen Bonifant, Challice Brenner, Daniel Cummings, Richard D Brenner, Malcolm K Ozcan, Ada Markovitz, David M Watanabe, Norihiro Thomas, Dafydd G Ashwood, Christopher |
| AuthorAffiliation | 3 Department of Internal Medicine , University of Michigan , Ann Arbor , Michigan , USA 4 Department of Pathology , University of Michigan , Ann Arbor , Michigan , USA 1 Center for Cell and Gene Therapy , Baylor College of Medicine , Houston , Texas , USA 5 Department of Surgery , Harvard Medical School , Boston , Massachusetts , USA 2 Department of Bioengineering , Rice University , Houston , Texas , USA 6 Department of Oncology, Sidney Kimmel Comprehensive Cancer Center , Johns Hopkins University School of Medicine , Baltimore , Maryland , USA |
| AuthorAffiliation_xml | – name: 1 Center for Cell and Gene Therapy , Baylor College of Medicine , Houston , Texas , USA – name: 3 Department of Internal Medicine , University of Michigan , Ann Arbor , Michigan , USA – name: 2 Department of Bioengineering , Rice University , Houston , Texas , USA – name: 5 Department of Surgery , Harvard Medical School , Boston , Massachusetts , USA – name: 4 Department of Pathology , University of Michigan , Ann Arbor , Michigan , USA – name: 6 Department of Oncology, Sidney Kimmel Comprehensive Cancer Center , Johns Hopkins University School of Medicine , Baltimore , Maryland , USA |
| Author_xml | – sequence: 1 givenname: Mary K orcidid: 0000-0002-2357-1733 surname: McKenna fullname: McKenna, Mary K email: mary.mckenna@bcm.edu organization: Center for Cell and Gene Therapy, Baylor College of Medicine, Houston, Texas, USA – sequence: 2 givenname: Ada surname: Ozcan fullname: Ozcan, Ada organization: Center for Cell and Gene Therapy, Baylor College of Medicine, Houston, Texas, USA – sequence: 3 givenname: Daniel surname: Brenner fullname: Brenner, Daniel organization: Department of Bioengineering, Rice University, Houston, Texas, USA – sequence: 4 givenname: Norihiro surname: Watanabe fullname: Watanabe, Norihiro organization: Center for Cell and Gene Therapy, Baylor College of Medicine, Houston, Texas, USA – sequence: 5 givenname: Maureen surname: Legendre fullname: Legendre, Maureen organization: Department of Internal Medicine, University of Michigan, Ann Arbor, Michigan, USA – sequence: 6 givenname: Dafydd G surname: Thomas fullname: Thomas, Dafydd G organization: Department of Pathology, University of Michigan, Ann Arbor, Michigan, USA – sequence: 7 givenname: Christopher surname: Ashwood fullname: Ashwood, Christopher organization: Department of Surgery, Harvard Medical School, Boston, Massachusetts, USA – sequence: 8 givenname: Richard D surname: Cummings fullname: Cummings, Richard D organization: Department of Surgery, Harvard Medical School, Boston, Massachusetts, USA – sequence: 9 givenname: Challice surname: Bonifant fullname: Bonifant, Challice organization: Department of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University School of Medicine, Baltimore, Maryland, USA – sequence: 10 givenname: David M surname: Markovitz fullname: Markovitz, David M organization: Department of Internal Medicine, University of Michigan, Ann Arbor, Michigan, USA – sequence: 11 givenname: Malcolm K surname: Brenner fullname: Brenner, Malcolm K organization: Center for Cell and Gene Therapy, Baylor College of Medicine, Houston, Texas, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/36653070$$D View this record in MEDLINE/PubMed |
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| PublicationDate | 2023-01-01 |
| PublicationDateYYYYMMDD | 2023-01-01 |
| PublicationDate_xml | – month: 01 year: 2023 text: 2023-01-01 day: 01 |
| PublicationDecade | 2020 |
| PublicationPlace | England |
| PublicationPlace_xml | – name: England – name: London – name: BMA House, Tavistock Square, London, WC1H 9JR |
| PublicationSeriesTitle | Original research |
| PublicationTitle | Journal for immunotherapy of cancer |
| PublicationTitleAbbrev | J Immunother Cancer |
| PublicationTitleAlternate | J Immunother Cancer |
| PublicationYear | 2023 |
| Publisher | BMJ Publishing Group Ltd BMJ Publishing Group LTD BMJ Publishing Group |
| Publisher_xml | – name: BMJ Publishing Group Ltd – name: BMJ Publishing Group LTD – name: BMJ Publishing Group |
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| Snippet | BackgroundCell therapies for solid tumors are thwarted by the hostile tumor microenvironment (TME) and by heterogeneous expression of tumor target antigens. We... Cell therapies for solid tumors are thwarted by the hostile tumor microenvironment (TME) and by heterogeneous expression of tumor target antigens. We address... Background Cell therapies for solid tumors are thwarted by the hostile tumor microenvironment (TME) and by heterogeneous expression of tumor target antigens.... |
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| SubjectTerms | Antibodies Antigens Cancer Carcinoma, Pancreatic Ductal Cells Flow cytometry Genotype & phenotype Hematology Humans Immune Cell Therapies and Immune Cell Engineering Immunotherapy Lectins Lectins - metabolism Lymphocytes Mass spectrometry Musa - metabolism Pancreatic cancer Pancreatic Neoplasms Receptors, Chimeric Antigen Receptors, Chimeric Antigen - genetics Receptors, Chimeric Antigen - metabolism Scientific imaging T-Lymphocytes Tumor Microenvironment Tumors |
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| Title | Novel banana lectin CAR-T cells to target pancreatic tumors and tumor-associated stroma |
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