CAR-CIK vs. CAR-T: benchmarking novel cytokine-induced killer cells as solid tumor immunotherapy in ErbB2+ rhabdomyosarcoma
IntroductionCAR-T cell therapy, though successful in hematologic malignancies, faces challenges in solid tumors due to limitations of autologous T cells. Cytokine-induced killer (CIK) cells can be given safely across allogeneic barriers and constitute alternative effector cells generated from health...
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2025-02-01
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| author | Laura M. Moser Laura M. Moser Laura M. Moser Laura M. Moser Laura M. Moser Catrin Heim Sebastian E. Koschade Sebastian E. Koschade Sebastian E. Koschade Sebastian E. Koschade Sebastian E. Koschade Philipp Wendel Philipp Wendel Philipp Wendel Philipp Wendel Süleyman Bozkurt Sabine Harenkamp Hermann Kreyenberg Hermann Kreyenberg Michael Merker Michael Merker Christian Münch Christian Münch Christian Münch Elise Gradhand Meike Vogler Meike Vogler Meike Vogler Evelyn Ullrich Evelyn Ullrich Evelyn Ullrich Evelyn Ullrich Evelyn Ullrich Halvard Bönig Halvard Bönig Jan-Henning Klusmann Jan-Henning Klusmann Jan-Henning Klusmann Jan-Henning Klusmann Peter Bader Peter Bader Peter Bader Peter Bader Peter Bader Winfried S. Wels Winfried S. Wels Winfried S. Wels Eva Rettinger Eva Rettinger Eva Rettinger Eva Rettinger Eva Rettinger |
| author_facet | Laura M. Moser Laura M. Moser Laura M. Moser Laura M. Moser Laura M. Moser Catrin Heim Sebastian E. Koschade Sebastian E. Koschade Sebastian E. Koschade Sebastian E. Koschade Sebastian E. Koschade Philipp Wendel Philipp Wendel Philipp Wendel Philipp Wendel Süleyman Bozkurt Sabine Harenkamp Hermann Kreyenberg Hermann Kreyenberg Michael Merker Michael Merker Christian Münch Christian Münch Christian Münch Elise Gradhand Meike Vogler Meike Vogler Meike Vogler Evelyn Ullrich Evelyn Ullrich Evelyn Ullrich Evelyn Ullrich Evelyn Ullrich Halvard Bönig Halvard Bönig Jan-Henning Klusmann Jan-Henning Klusmann Jan-Henning Klusmann Jan-Henning Klusmann Peter Bader Peter Bader Peter Bader Peter Bader Peter Bader Winfried S. Wels Winfried S. Wels Winfried S. Wels Eva Rettinger Eva Rettinger Eva Rettinger Eva Rettinger Eva Rettinger |
| author_sort | Laura M. Moser |
| collection | DOAJ |
| description | IntroductionCAR-T cell therapy, though successful in hematologic malignancies, faces challenges in solid tumors due to limitations of autologous T cells. Cytokine-induced killer (CIK) cells can be given safely across allogeneic barriers and constitute alternative effector cells generated from healthy donors. CIK cells are a heterogenous population of predominantly T cells with a mixed natural killer (NK) phenotype and combine non-MHC-restricted cytotoxicity with potent anti-tumor capacity of the adaptive immune system. Here, we characterize and compare efficacy, phenotypic subpopulations and modes of action of CAR-CIK cells and conventional CAR-T cells from same-donor samples in ErbB2+ rhabdomyosarcoma (RMS).MethodsTo benchmark CAR-CIK against conventional CAR-T cells, effector cells were generated from same-donor samples and lentivirally transduced with a second generation CD28-CD3ζ CAR. Effector subpopulations and their dynamics upon target cell exposure were phenotypically characterized by flow cytometry. Efficacy was assessed in human ErbB2+ RMS cancer cell lines and primary patient samples in vitro and ex vivo using cytotoxicity and spheroid co-incubation assays. Modes of action were assessed by comparing cytokine secretion profiles using bead-based multiplexed flow cytometry and by liquid chromatography mass spectrometry whole cell proteomics. Finally, we used an in vivo model of RMS mimicking minimal metastatic residual disease to compare anti-tumor potency of CAR-CIK vs. CAR-T cells and to assess their target organ infiltration.ResultsIn vitro assays demonstrated superior cytotoxicity of CAR-CIK cells against RMS cell lines and primary tumor samples. Long-term co-incubation with tumor spheroids led to expansion of CAR-CIK cells and enrichment of CD3+CD56+ TNK cells. CAR-CIK cell cytokine signature showed significantly increased secretion of effector molecules like interferon-γ, perforin and granulysin, and lower secretion of Th2 cytokines IL-2, IL-4 and IL-10. Whole cell proteomics showed corresponding upregulation of chemokine signaling and NK-cytotoxicity pathways in CAR-CIK cells. In NSG mice xenografted with ErbB2+ RMS, a single injection of either CAR-effector cells strongly impeded metastatic tumor development and significantly improved survival.ConclusionOur results demonstrate that CAR-CIK cells are at least equipotent to CAR-T cells. Combined with their favorable safety profile and allogeneic applicability, these findings position CAR-CIK cells as promising immune effectors for solid tumors. |
| format | Article |
| id | doaj-art-dc4bea898f8f4b188f2485cd1a023539 |
| institution | Kabale University |
| issn | 1664-3224 |
| language | English |
| publishDate | 2025-02-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Immunology |
| spelling | doaj-art-dc4bea898f8f4b188f2485cd1a0235392025-02-03T10:47:36ZengFrontiers Media S.A.Frontiers in Immunology1664-32242025-02-011610.3389/fimmu.2025.14858171485817CAR-CIK vs. CAR-T: benchmarking novel cytokine-induced killer cells as solid tumor immunotherapy in ErbB2+ rhabdomyosarcomaLaura M. Moser0Laura M. Moser1Laura M. Moser2Laura M. Moser3Laura M. Moser4Catrin Heim5Sebastian E. Koschade6Sebastian E. Koschade7Sebastian E. Koschade8Sebastian E. Koschade9Sebastian E. Koschade10Philipp Wendel11Philipp Wendel12Philipp Wendel13Philipp Wendel14Süleyman Bozkurt15Sabine Harenkamp16Hermann Kreyenberg17Hermann Kreyenberg18Michael Merker19Michael Merker20Christian Münch21Christian Münch22Christian Münch23Elise Gradhand24Meike Vogler25Meike Vogler26Meike Vogler27Evelyn Ullrich28Evelyn Ullrich29Evelyn Ullrich30Evelyn Ullrich31Evelyn Ullrich32Halvard Bönig33Halvard Bönig34Jan-Henning Klusmann35Jan-Henning Klusmann36Jan-Henning Klusmann37Jan-Henning Klusmann38Peter Bader39Peter Bader40Peter Bader41Peter Bader42Peter Bader43Winfried S. Wels44Winfried S. Wels45Winfried S. Wels46Eva Rettinger47Eva Rettinger48Eva Rettinger49Eva Rettinger50Eva Rettinger51Division for Stem Cell Transplantation and Immunology, Department of Pediatrics, Goethe University Frankfurt, Frankfurt am Main, GermanyDepartment of Pediatrics, Goethe University Frankfurt, Frankfurt am Main, GermanyGerman Cancer Consortium (DKTK), partner site Frankfurt/Mainz, Frankfurt am Main, GermanyFrankfurt Cancer Institute (FCI), Goethe University, Frankfurt am Main, GermanyUniversitäres Centrum für Tumorerkrankungen (UCT), Frankfurt am Main, GermanyDivision for Stem Cell Transplantation and Immunology, Department of Pediatrics, Goethe University Frankfurt, Frankfurt am Main, GermanyGerman Cancer Consortium (DKTK), partner site Frankfurt/Mainz, Frankfurt am Main, GermanyFrankfurt Cancer Institute (FCI), Goethe University, Frankfurt am Main, GermanyUniversitäres Centrum für Tumorerkrankungen (UCT), Frankfurt am Main, GermanyDepartment of Medicine, Hematology/Oncology, Goethe University Frankfurt, Frankfurt am Main, GermanyInstitute of Biochemistry II, Faculty of Medicine, Goethe University, Frankfurt am Main, GermanyDepartment of Pediatrics, Goethe University Frankfurt, Frankfurt am Main, GermanyGerman Cancer Consortium (DKTK), partner site Frankfurt/Mainz, Frankfurt am Main, GermanyExperimental Immunology & Cell Therapy, Department of Pediatrics, Goethe University, Frankfurt am Main, GermanyInstitute for Organic Chemistry and Biochemistry, Technical University of Darmstadt, Darmstadt, GermanyInstitute of Biochemistry II, Faculty of Medicine, Goethe University, Frankfurt am Main, Germany0Department of Cellular Therapeutics/Cell Processing, Institute for Transfusion Medicine and Immunotherapy, Goethe University, Frankfurt am Main, GermanyDivision for Stem Cell Transplantation and Immunology, Department of Pediatrics, Goethe University Frankfurt, Frankfurt am Main, GermanyDepartment of Pediatrics, Goethe University Frankfurt, Frankfurt am Main, GermanyDivision for Stem Cell Transplantation and Immunology, Department of Pediatrics, Goethe University Frankfurt, Frankfurt am Main, GermanyDepartment of Pediatrics, Goethe University Frankfurt, Frankfurt am Main, GermanyFrankfurt Cancer Institute (FCI), Goethe University, Frankfurt am Main, GermanyInstitute of Biochemistry II, Faculty of Medicine, Goethe University, Frankfurt am Main, Germany1Cardio-Pulmonary Institute, Frankfurt am Main, Germany2Department of Pediatric and Perinatal Pathology, Dr. Senckenberg Institute of Pathology, Goethe-University Frankfurt, Frankfurt am Main, GermanyGerman Cancer Consortium (DKTK), partner site Frankfurt/Mainz, Frankfurt am Main, GermanyFrankfurt Cancer Institute (FCI), Goethe University, Frankfurt am Main, Germany3Institute for Experimental Pediatric Hematology and Oncology, Goethe University, Frankfurt am Main, GermanyDepartment of Pediatrics, Goethe University Frankfurt, Frankfurt am Main, GermanyGerman Cancer Consortium (DKTK), partner site Frankfurt/Mainz, Frankfurt am Main, GermanyFrankfurt Cancer Institute (FCI), Goethe University, Frankfurt am Main, GermanyUniversitäres Centrum für Tumorerkrankungen (UCT), Frankfurt am Main, GermanyExperimental Immunology & Cell Therapy, Department of Pediatrics, Goethe University, Frankfurt am Main, Germany0Department of Cellular Therapeutics/Cell Processing, Institute for Transfusion Medicine and Immunotherapy, Goethe University, Frankfurt am Main, Germany4Division of Hematology, Department of Medicine, University of Washington, Seattle, WA, United StatesDepartment of Pediatrics, Goethe University Frankfurt, Frankfurt am Main, GermanyGerman Cancer Consortium (DKTK), partner site Frankfurt/Mainz, Frankfurt am Main, GermanyFrankfurt Cancer Institute (FCI), Goethe University, Frankfurt am Main, GermanyUniversitäres Centrum für Tumorerkrankungen (UCT), Frankfurt am Main, GermanyDivision for Stem Cell Transplantation and Immunology, Department of Pediatrics, Goethe University Frankfurt, Frankfurt am Main, GermanyDepartment of Pediatrics, Goethe University Frankfurt, Frankfurt am Main, GermanyGerman Cancer Consortium (DKTK), partner site Frankfurt/Mainz, Frankfurt am Main, GermanyFrankfurt Cancer Institute (FCI), Goethe University, Frankfurt am Main, GermanyUniversitäres Centrum für Tumorerkrankungen (UCT), Frankfurt am Main, GermanyGerman Cancer Consortium (DKTK), partner site Frankfurt/Mainz, Frankfurt am Main, GermanyFrankfurt Cancer Institute (FCI), Goethe University, Frankfurt am Main, Germany5Georg-Speyer-Haus, Institute for Tumor Biology and Experimental Therapy, Frankfurt am Main, GermanyDivision for Stem Cell Transplantation and Immunology, Department of Pediatrics, Goethe University Frankfurt, Frankfurt am Main, GermanyDepartment of Pediatrics, Goethe University Frankfurt, Frankfurt am Main, GermanyGerman Cancer Consortium (DKTK), partner site Frankfurt/Mainz, Frankfurt am Main, GermanyFrankfurt Cancer Institute (FCI), Goethe University, Frankfurt am Main, GermanyUniversitäres Centrum für Tumorerkrankungen (UCT), Frankfurt am Main, GermanyIntroductionCAR-T cell therapy, though successful in hematologic malignancies, faces challenges in solid tumors due to limitations of autologous T cells. Cytokine-induced killer (CIK) cells can be given safely across allogeneic barriers and constitute alternative effector cells generated from healthy donors. CIK cells are a heterogenous population of predominantly T cells with a mixed natural killer (NK) phenotype and combine non-MHC-restricted cytotoxicity with potent anti-tumor capacity of the adaptive immune system. Here, we characterize and compare efficacy, phenotypic subpopulations and modes of action of CAR-CIK cells and conventional CAR-T cells from same-donor samples in ErbB2+ rhabdomyosarcoma (RMS).MethodsTo benchmark CAR-CIK against conventional CAR-T cells, effector cells were generated from same-donor samples and lentivirally transduced with a second generation CD28-CD3ζ CAR. Effector subpopulations and their dynamics upon target cell exposure were phenotypically characterized by flow cytometry. Efficacy was assessed in human ErbB2+ RMS cancer cell lines and primary patient samples in vitro and ex vivo using cytotoxicity and spheroid co-incubation assays. Modes of action were assessed by comparing cytokine secretion profiles using bead-based multiplexed flow cytometry and by liquid chromatography mass spectrometry whole cell proteomics. Finally, we used an in vivo model of RMS mimicking minimal metastatic residual disease to compare anti-tumor potency of CAR-CIK vs. CAR-T cells and to assess their target organ infiltration.ResultsIn vitro assays demonstrated superior cytotoxicity of CAR-CIK cells against RMS cell lines and primary tumor samples. Long-term co-incubation with tumor spheroids led to expansion of CAR-CIK cells and enrichment of CD3+CD56+ TNK cells. CAR-CIK cell cytokine signature showed significantly increased secretion of effector molecules like interferon-γ, perforin and granulysin, and lower secretion of Th2 cytokines IL-2, IL-4 and IL-10. Whole cell proteomics showed corresponding upregulation of chemokine signaling and NK-cytotoxicity pathways in CAR-CIK cells. In NSG mice xenografted with ErbB2+ RMS, a single injection of either CAR-effector cells strongly impeded metastatic tumor development and significantly improved survival.ConclusionOur results demonstrate that CAR-CIK cells are at least equipotent to CAR-T cells. Combined with their favorable safety profile and allogeneic applicability, these findings position CAR-CIK cells as promising immune effectors for solid tumors.https://www.frontiersin.org/articles/10.3389/fimmu.2025.1485817/fullcytokine-induced killer cells (CIK)CAR-Trhabdomyosarcomasolid tumorsERBB2 |
| spellingShingle | Laura M. Moser Laura M. Moser Laura M. Moser Laura M. Moser Laura M. Moser Catrin Heim Sebastian E. Koschade Sebastian E. Koschade Sebastian E. Koschade Sebastian E. Koschade Sebastian E. Koschade Philipp Wendel Philipp Wendel Philipp Wendel Philipp Wendel Süleyman Bozkurt Sabine Harenkamp Hermann Kreyenberg Hermann Kreyenberg Michael Merker Michael Merker Christian Münch Christian Münch Christian Münch Elise Gradhand Meike Vogler Meike Vogler Meike Vogler Evelyn Ullrich Evelyn Ullrich Evelyn Ullrich Evelyn Ullrich Evelyn Ullrich Halvard Bönig Halvard Bönig Jan-Henning Klusmann Jan-Henning Klusmann Jan-Henning Klusmann Jan-Henning Klusmann Peter Bader Peter Bader Peter Bader Peter Bader Peter Bader Winfried S. Wels Winfried S. Wels Winfried S. Wels Eva Rettinger Eva Rettinger Eva Rettinger Eva Rettinger Eva Rettinger CAR-CIK vs. CAR-T: benchmarking novel cytokine-induced killer cells as solid tumor immunotherapy in ErbB2+ rhabdomyosarcoma Frontiers in Immunology cytokine-induced killer cells (CIK) CAR-T rhabdomyosarcoma solid tumors ERBB2 |
| title | CAR-CIK vs. CAR-T: benchmarking novel cytokine-induced killer cells as solid tumor immunotherapy in ErbB2+ rhabdomyosarcoma |
| title_full | CAR-CIK vs. CAR-T: benchmarking novel cytokine-induced killer cells as solid tumor immunotherapy in ErbB2+ rhabdomyosarcoma |
| title_fullStr | CAR-CIK vs. CAR-T: benchmarking novel cytokine-induced killer cells as solid tumor immunotherapy in ErbB2+ rhabdomyosarcoma |
| title_full_unstemmed | CAR-CIK vs. CAR-T: benchmarking novel cytokine-induced killer cells as solid tumor immunotherapy in ErbB2+ rhabdomyosarcoma |
| title_short | CAR-CIK vs. CAR-T: benchmarking novel cytokine-induced killer cells as solid tumor immunotherapy in ErbB2+ rhabdomyosarcoma |
| title_sort | car cik vs car t benchmarking novel cytokine induced killer cells as solid tumor immunotherapy in erbb2 rhabdomyosarcoma |
| topic | cytokine-induced killer cells (CIK) CAR-T rhabdomyosarcoma solid tumors ERBB2 |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2025.1485817/full |
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