TRAIL-dependent apoptosis of peritoneal mesothelial cells by NK cells promotes ovarian cancer invasion
A crucial requirement for metastasis formation in ovarian high-grade serous carcinoma (HGSC) is the disruption of the protective peritoneal mesothelium. Using co-culture systems of primary human cells, we discovered that tumor-associated NK cells induce TRAIL-dependent apoptosis in mesothelial cells...
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| Published in: | iScience Vol. 26; no. 12; p. 108401 |
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| Main Authors: | , , , , , , , , , , , , , , , |
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15-12-2023
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| Abstract | A crucial requirement for metastasis formation in ovarian high-grade serous carcinoma (HGSC) is the disruption of the protective peritoneal mesothelium. Using co-culture systems of primary human cells, we discovered that tumor-associated NK cells induce TRAIL-dependent apoptosis in mesothelial cells via death receptors DR4 and DR5 upon encounter with activated T cells. Upregulation of TRAIL expression in NK cells concomitant with enhanced cytotoxicity toward mesothelial cells was driven predominantly by T-cell-derived TNFα, as shown by affinity proteomics-based analysis of the T cell secretome in conjunction with functional studies. Consistent with these findings, we detected apoptotic mesothelial cells in the peritoneal fluid of HGSC patients. In contrast to mesothelial cells, HGSC cells express negligible levels of both DR4 and DR5 and are TRAIL resistant, indicating cell-type-selective killing by NK cells. Our data point to a cooperative action of T and NK in breaching the mesothelial barrier in HGSC patients.
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•Cancer-associated NK cells induce TRAIL-dependent apoptosis in mesothelial cells•Induction of apoptosis by NK cells is mainly driven by T-cell-derived TNFα•NK-cell-mediated mesothelial cell death promotes ovarian cancer cell invasion•Low TRAIL receptor levels on cancer cells contribute to their TRAIL resistance
Microenvironment; Immunology; Cancer |
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| AbstractList | A crucial requirement for metastasis formation in ovarian high-grade serous carcinoma (HGSC) is the disruption of the protective peritoneal mesothelium. Using co-culture systems of primary human cells, we discovered that tumor-associated NK cells induce TRAIL-dependent apoptosis in mesothelial cells via death receptors DR4 and DR5 upon encounter with activated T cells. Upregulation of TRAIL expression in NK cells concomitant with enhanced cytotoxicity toward mesothelial cells was driven predominantly by T-cell-derived TNFα, as shown by affinity proteomics-based analysis of the T cell secretome in conjunction with functional studies. Consistent with these findings, we detected apoptotic mesothelial cells in the peritoneal fluid of HGSC patients. In contrast to mesothelial cells, HGSC cells express negligible levels of both DR4 and DR5 and are TRAIL resistant, indicating cell-type-selective killing by NK cells. Our data point to a cooperative action of T and NK in breaching the mesothelial barrier in HGSC patients.
[Display omitted]
•Cancer-associated NK cells induce TRAIL-dependent apoptosis in mesothelial cells•Induction of apoptosis by NK cells is mainly driven by T-cell-derived TNFα•NK-cell-mediated mesothelial cell death promotes ovarian cancer cell invasion•Low TRAIL receptor levels on cancer cells contribute to their TRAIL resistance
Microenvironment; Immunology; Cancer A crucial requirement for metastasis formation in ovarian high-grade serous carcinoma (HGSC) is the disruption of the protective peritoneal mesothelium. Using co-culture systems of primary human cells, we discovered that tumor-associated NK cells induce TRAIL-dependent apoptosis in mesothelial cells via death receptors DR4 and DR5 upon encounter with activated T cells. Upregulation of TRAIL expression in NK cells concomitant with enhanced cytotoxicity toward mesothelial cells was driven predominantly by T-cell-derived TNFα, as shown by affinity proteomics-based analysis of the T cell secretome in conjunction with functional studies. Consistent with these findings, we detected apoptotic mesothelial cells in the peritoneal fluid of HGSC patients. In contrast to mesothelial cells, HGSC cells express negligible levels of both DR4 and DR5 and are TRAIL resistant, indicating cell-type-selective killing by NK cells. Our data point to a cooperative action of T and NK in breaching the mesothelial barrier in HGSC patients. • Cancer-associated NK cells induce TRAIL-dependent apoptosis in mesothelial cells • Induction of apoptosis by NK cells is mainly driven by T-cell-derived TNFα • NK-cell-mediated mesothelial cell death promotes ovarian cancer cell invasion • Low TRAIL receptor levels on cancer cells contribute to their TRAIL resistance Microenvironment; Immunology; Cancer A crucial requirement for metastasis formation in ovarian high-grade serous carcinoma (HGSC) is the disruption of the protective peritoneal mesothelium. Using co-culture systems of primary human cells, we discovered that tumor-associated NK cells induce TRAIL-dependent apoptosis in mesothelial cells via death receptors DR4 and DR5 upon encounter with activated T cells. Upregulation of TRAIL expression in NK cells concomitant with enhanced cytotoxicity toward mesothelial cells was driven predominantly by T-cell-derived TNFα, as shown by affinity proteomics-based analysis of the T cell secretome in conjunction with functional studies. Consistent with these findings, we detected apoptotic mesothelial cells in the peritoneal fluid of HGSC patients. In contrast to mesothelial cells, HGSC cells express negligible levels of both DR4 and DR5 and are TRAIL resistant, indicating cell-type-selective killing by NK cells. Our data point to a cooperative action of T and NK in breaching the mesothelial barrier in HGSC patients. A crucial requirement for metastasis formation in ovarian high-grade serous carcinoma (HGSC) is the disruption of the protective peritoneal mesothelium. Using co-culture systems of primary human cells, we discovered that tumor-associated NK cells induce TRAIL-dependent apoptosis in mesothelial cells via death receptors DR4 and DR5 upon encounter with activated T cells. Upregulation of TRAIL expression in NK cells concomitant with enhanced cytotoxicity toward mesothelial cells was driven predominantly by T-cell-derived TNFα, as shown by affinity proteomics-based analysis of the T cell secretome in conjunction with functional studies. Consistent with these findings, we detected apoptotic mesothelial cells in the peritoneal fluid of HGSC patients. In contrast to mesothelial cells, HGSC cells express negligible levels of both DR4 and DR5 and are TRAIL resistant, indicating cell-type-selective killing by NK cells. Our data point to a cooperative action of T and NK in breaching the mesothelial barrier in HGSC patients. |
| ArticleNumber | 108401 |
| Author | Wagner, Uwe Müller, Rolf Finkernagel, Florian Pogge von Strandmann, Elke Steitz, Anna Mary Worzfeld, Thomas Knuth, Isabel Jansen, Julia M. Müller-Brüsselbach, Sabine Schröder, Clarissa Huber, Magdalena Keber, Corinna U. Reinartz, Silke Sommerfeld, Leah Graumann, Johannes Beutgen, Vanessa M. |
| Author_xml | – sequence: 1 givenname: Anna Mary surname: Steitz fullname: Steitz, Anna Mary organization: Translational Oncology Group, Center for Tumor Biology and Immunology (ZTI), Philipps University, 35043 Marburg, Germany – sequence: 2 givenname: Clarissa surname: Schröder fullname: Schröder, Clarissa organization: Translational Oncology Group, Center for Tumor Biology and Immunology (ZTI), Philipps University, 35043 Marburg, Germany – sequence: 3 givenname: Isabel surname: Knuth fullname: Knuth, Isabel organization: Translational Oncology Group, Center for Tumor Biology and Immunology (ZTI), Philipps University, 35043 Marburg, Germany – sequence: 4 givenname: Corinna U. surname: Keber fullname: Keber, Corinna U. organization: Institute for Pathology, Philipps University, 35043 Marburg, Germany – sequence: 5 givenname: Leah surname: Sommerfeld fullname: Sommerfeld, Leah organization: Translational Oncology Group, Center for Tumor Biology and Immunology (ZTI), Philipps University, 35043 Marburg, Germany – sequence: 6 givenname: Florian surname: Finkernagel fullname: Finkernagel, Florian organization: Translational Oncology Group, Center for Tumor Biology and Immunology (ZTI), Philipps University, 35043 Marburg, Germany – sequence: 7 givenname: Julia M. surname: Jansen fullname: Jansen, Julia M. organization: Clinic for Gynecology, Gynecological Oncology, Gynecological Endocrinology, University Hospital (UKGM), 35043 Marburg, Germany – sequence: 8 givenname: Uwe surname: Wagner fullname: Wagner, Uwe organization: Clinic for Gynecology, Gynecological Oncology, Gynecological Endocrinology, University Hospital (UKGM), 35043 Marburg, Germany – sequence: 9 givenname: Sabine surname: Müller-Brüsselbach fullname: Müller-Brüsselbach, Sabine organization: Translational Oncology Group, Center for Tumor Biology and Immunology (ZTI), Philipps University, 35043 Marburg, Germany – sequence: 10 givenname: Thomas surname: Worzfeld fullname: Worzfeld, Thomas organization: Institute of Pharmacology, Biochemical-Pharmacological Center (BPC), Philipps University, 35043 Marburg, Germany – sequence: 11 givenname: Magdalena surname: Huber fullname: Huber, Magdalena organization: Institute of Systems Immunology, Center for Tumor Biology and Immunology (ZTI), Philipps University, 35043 Marburg, Germany – sequence: 12 givenname: Vanessa M. surname: Beutgen fullname: Beutgen, Vanessa M. organization: Institute of Translational Proteomics, Philipps University, 35043 Marburg, Germany – sequence: 13 givenname: Johannes surname: Graumann fullname: Graumann, Johannes organization: Institute of Translational Proteomics, Philipps University, 35043 Marburg, Germany – sequence: 14 givenname: Elke surname: Pogge von Strandmann fullname: Pogge von Strandmann, Elke organization: Institute for Tumor Immunology, Center for Tumor Biology and Immunology (ZTI), Clinic for Hematology, Oncology and Immunology, Philipps University, 35043 Marburg, Germany – sequence: 15 givenname: Rolf surname: Müller fullname: Müller, Rolf email: rolf.mueller@uni-marburg.de organization: Translational Oncology Group, Center for Tumor Biology and Immunology (ZTI), Philipps University, 35043 Marburg, Germany – sequence: 16 givenname: Silke surname: Reinartz fullname: Reinartz, Silke email: silke.reinartz@uni-marburg.de organization: Translational Oncology Group, Center for Tumor Biology and Immunology (ZTI), Philipps University, 35043 Marburg, Germany |
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| CitedBy_id | crossref_primary_10_1021_acs_analchem_3c04116 crossref_primary_10_1002_ctm2_1604 crossref_primary_10_3389_fimmu_2024_1412328 crossref_primary_10_3390_cells13060521 |
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| Keywords | Immunology Microenvironment Cancer |
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