Neutrophils Kill Antibody-Opsonized Cancer Cells by Trogoptosis
Destruction of cancer cells by therapeutic antibodies occurs, at least in part, through antibody-dependent cellular cytotoxicity (ADCC), and this can be mediated by various Fc-receptor-expressing immune cells, including neutrophils. However, the mechanism(s) by which neutrophils kill antibody-opsoni...
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| Published in: | Cell reports (Cambridge) Vol. 23; no. 13; pp. 3946 - 3959.e6 |
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| Language: | English |
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26.06.2018
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| ISSN: | 2211-1247, 2211-1247 |
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| Abstract | Destruction of cancer cells by therapeutic antibodies occurs, at least in part, through antibody-dependent cellular cytotoxicity (ADCC), and this can be mediated by various Fc-receptor-expressing immune cells, including neutrophils. However, the mechanism(s) by which neutrophils kill antibody-opsonized cancer cells has not been established. Here, we demonstrate that neutrophils can exert a mode of destruction of cancer cells, which involves antibody-mediated trogocytosis by neutrophils. Intimately associated with this is an active mechanical disruption of the cancer cell plasma membrane, leading to a lytic (i.e., necrotic) type of cancer cell death. Furthermore, this mode of destruction of antibody-opsonized cancer cells by neutrophils is potentiated by CD47-SIRPα checkpoint blockade. Collectively, these findings show that neutrophil ADCC toward cancer cells occurs by a mechanism of cytotoxicity called trogoptosis, which can be further improved by targeting CD47-SIRPα interactions.
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•Neutrophils kill antibody-opsonized cancer cells by a process called trogoptosis•Cancer cell plasma membrane ingestion by neutrophils is instrumental in trogoptosis•Trogoptosis by neutrophils is further enhanced by CD47-SIRPα checkpoint inhibition
Matlung et al. identify trogoptosis as an immune cell-mediated mechanism of cytotoxicity, demonstrating that neutrophil-mediated destruction of antibody-opsonized cancer cells occurs through a specific process that is distinct from that used by other immune cells. |
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| AbstractList | Destruction of cancer cells by therapeutic antibodies occurs, at least in part, through antibody-dependent cellular cytotoxicity (ADCC), and this can be mediated by various Fc-receptor-expressing immune cells, including neutrophils. However, the mechanism(s) by which neutrophils kill antibody-opsonized cancer cells has not been established. Here, we demonstrate that neutrophils can exert a mode of destruction of cancer cells, which involves antibody-mediated trogocytosis by neutrophils. Intimately associated with this is an active mechanical disruption of the cancer cell plasma membrane, leading to a lytic (i.e., necrotic) type of cancer cell death. Furthermore, this mode of destruction of antibody-opsonized cancer cells by neutrophils is potentiated by CD47-SIRPα checkpoint blockade. Collectively, these findings show that neutrophil ADCC toward cancer cells occurs by a mechanism of cytotoxicity called trogoptosis, which can be further improved by targeting CD47-SIRPα interactions.
[Display omitted]
•Neutrophils kill antibody-opsonized cancer cells by a process called trogoptosis•Cancer cell plasma membrane ingestion by neutrophils is instrumental in trogoptosis•Trogoptosis by neutrophils is further enhanced by CD47-SIRPα checkpoint inhibition
Matlung et al. identify trogoptosis as an immune cell-mediated mechanism of cytotoxicity, demonstrating that neutrophil-mediated destruction of antibody-opsonized cancer cells occurs through a specific process that is distinct from that used by other immune cells. Destruction of cancer cells by therapeutic antibodies occurs, at least in part, through antibody-dependent cellular cytotoxicity (ADCC), and this can be mediated by various Fc-receptor-expressing immune cells, including neutrophils. However, the mechanism(s) by which neutrophils kill antibody-opsonized cancer cells has not been established. Here, we demonstrate that neutrophils can exert a mode of destruction of cancer cells, which involves antibody-mediated trogocytosis by neutrophils. Intimately associated with this is an active mechanical disruption of the cancer cell plasma membrane, leading to a lytic (i.e., necrotic) type of cancer cell death. Furthermore, this mode of destruction of antibody-opsonized cancer cells by neutrophils is potentiated by CD47-SIRPα checkpoint blockade. Collectively, these findings show that neutrophil ADCC toward cancer cells occurs by a mechanism of cytotoxicity called trogoptosis, which can be further improved by targeting CD47-SIRPα interactions. : Matlung et al. identify trogoptosis as an immune cell-mediated mechanism of cytotoxicity, demonstrating that neutrophil-mediated destruction of antibody-opsonized cancer cells occurs through a specific process that is distinct from that used by other immune cells. Keywords: antibody-dependent cellular cytotoxicity, neutrophils, CD47-SIRPα interaction, trogocytosis, trogoptosis Destruction of cancer cells by therapeutic antibodies occurs, at least in part, through antibody-dependent cellular cytotoxicity (ADCC), and this can be mediated by various Fc-receptor-expressing immune cells, including neutrophils. However, the mechanism(s) by which neutrophils kill antibody-opsonized cancer cells has not been established. Here, we demonstrate that neutrophils can exert a mode of destruction of cancer cells, which involves antibody-mediated trogocytosis by neutrophils. Intimately associated with this is an active mechanical disruption of the cancer cell plasma membrane, leading to a lytic (i.e., necrotic) type of cancer cell death. Furthermore, this mode of destruction of antibody-opsonized cancer cells by neutrophils is potentiated by CD47-SIRPα checkpoint blockade. Collectively, these findings show that neutrophil ADCC toward cancer cells occurs by a mechanism of cytotoxicity called trogoptosis, which can be further improved by targeting CD47-SIRPα interactions.Destruction of cancer cells by therapeutic antibodies occurs, at least in part, through antibody-dependent cellular cytotoxicity (ADCC), and this can be mediated by various Fc-receptor-expressing immune cells, including neutrophils. However, the mechanism(s) by which neutrophils kill antibody-opsonized cancer cells has not been established. Here, we demonstrate that neutrophils can exert a mode of destruction of cancer cells, which involves antibody-mediated trogocytosis by neutrophils. Intimately associated with this is an active mechanical disruption of the cancer cell plasma membrane, leading to a lytic (i.e., necrotic) type of cancer cell death. Furthermore, this mode of destruction of antibody-opsonized cancer cells by neutrophils is potentiated by CD47-SIRPα checkpoint blockade. Collectively, these findings show that neutrophil ADCC toward cancer cells occurs by a mechanism of cytotoxicity called trogoptosis, which can be further improved by targeting CD47-SIRPα interactions. Destruction of cancer cells by therapeutic antibodies occurs, at least in part, through antibody-dependent cellular cytotoxicity (ADCC), and this can be mediated by various Fc-receptor-expressing immune cells, including neutrophils. However, the mechanism(s) by which neutrophils kill antibody-opsonized cancer cells has not been established. Here, we demonstrate that neutrophils can exert a mode of destruction of cancer cells, which involves antibody-mediated trogocytosis by neutrophils. Intimately associated with this is an active mechanical disruption of the cancer cell plasma membrane, leading to a lytic (i.e., necrotic) type of cancer cell death. Furthermore, this mode of destruction of antibody-opsonized cancer cells by neutrophils is potentiated by CD47-SIRPα checkpoint blockade. Collectively, these findings show that neutrophil ADCC toward cancer cells occurs by a mechanism of cytotoxicity called trogoptosis, which can be further improved by targeting CD47-SIRPα interactions. |
| Author | Verkuijlen, Paul Beijersbergen, Roderick L. van Bruggen, Robin van Rees, Dieke J. Menke-van der Houven van Oordt, Catharina Willemien van Lier, Rene A.W. Schornagel, Karin Seeger, Karl Boelens, Jaap J. Leusen, Jeanette H.W. Matlung, Hanke L. Kuhnle, Ingrid van der Werff Ten Bosch, Jutte Franke, Katka Lieftink, Cor Kubes, Paul Kuijpers, Taco W. Roos, Dirk Rutella, Sergio Babes, Liane Halonen, Pasi van den Berg, Timo K. Treffers, Louise W. Pagliara, Daria Zhao, Xi Wen Suzuki, Eiji van Houdt, Michel Janssen, Hans Matozaki, Takashi |
| Author_xml | – sequence: 1 givenname: Hanke L. surname: Matlung fullname: Matlung, Hanke L. organization: Sanquin Research, and Landsteiner Laboratory, Academic Medical Center, University of Amsterdam, Amsterdam, the Netherlands – sequence: 2 givenname: Liane surname: Babes fullname: Babes, Liane organization: Immunology Research Group, University of Calgary, Calgary, Alberta, Canada – sequence: 3 givenname: Xi Wen surname: Zhao fullname: Zhao, Xi Wen organization: Sanquin Research, and Landsteiner Laboratory, Academic Medical Center, University of Amsterdam, Amsterdam, the Netherlands – sequence: 4 givenname: Michel surname: van Houdt fullname: van Houdt, Michel organization: Sanquin Research, and Landsteiner Laboratory, Academic Medical Center, University of Amsterdam, Amsterdam, the Netherlands – sequence: 5 givenname: Louise W. surname: Treffers fullname: Treffers, Louise W. organization: Sanquin Research, and Landsteiner Laboratory, Academic Medical Center, University of Amsterdam, Amsterdam, the Netherlands – sequence: 6 givenname: Dieke J. surname: van Rees fullname: van Rees, Dieke J. organization: Sanquin Research, and Landsteiner Laboratory, Academic Medical Center, University of Amsterdam, Amsterdam, the Netherlands – sequence: 7 givenname: Katka surname: Franke fullname: Franke, Katka organization: Sanquin Research, and Landsteiner Laboratory, Academic Medical Center, University of Amsterdam, Amsterdam, the Netherlands – sequence: 8 givenname: Karin surname: Schornagel fullname: Schornagel, Karin organization: Sanquin Research, and Landsteiner Laboratory, Academic Medical Center, University of Amsterdam, Amsterdam, the Netherlands – sequence: 9 givenname: Paul surname: Verkuijlen fullname: Verkuijlen, Paul organization: Sanquin Research, and Landsteiner Laboratory, Academic Medical Center, University of Amsterdam, Amsterdam, the Netherlands – sequence: 10 givenname: Hans surname: Janssen fullname: Janssen, Hans organization: Division of Cell Biology, the Netherlands Cancer Institute, Amsterdam, the Netherlands – sequence: 11 givenname: Pasi surname: Halonen fullname: Halonen, Pasi organization: Division of Molecular Carcinogenesis and the NKI Robotics and Screening Center, the Netherlands Cancer Institute, Amsterdam, the Netherlands – sequence: 12 givenname: Cor surname: Lieftink fullname: Lieftink, Cor organization: Division of Molecular Carcinogenesis and the NKI Robotics and Screening Center, the Netherlands Cancer Institute, Amsterdam, the Netherlands – sequence: 13 givenname: Roderick L. surname: Beijersbergen fullname: Beijersbergen, Roderick L. organization: Division of Molecular Carcinogenesis and the NKI Robotics and Screening Center, the Netherlands Cancer Institute, Amsterdam, the Netherlands – sequence: 14 givenname: Jeanette H.W. surname: Leusen fullname: Leusen, Jeanette H.W. organization: Immunotherapy Laboratory, Laboratory for Translational Immunology, University Medical Center Utrecht, Utrecht, the Netherlands – sequence: 15 givenname: Jaap J. surname: Boelens fullname: Boelens, Jaap J. organization: U-DANCE, Laboratory for Translational Immunology, UMC Utrecht, Utrecht, the Netherlands – sequence: 16 givenname: Ingrid surname: Kuhnle fullname: Kuhnle, Ingrid organization: Department of Pediatrics, University Medicine Göttingen, Göttingen, Germany – sequence: 17 givenname: Jutte surname: van der Werff Ten Bosch fullname: van der Werff Ten Bosch, Jutte organization: Department of Pediatrics, Universitair Ziekenhuis Brussel, Brussels, Belgium – sequence: 18 givenname: Karl surname: Seeger fullname: Seeger, Karl organization: Department of Pediatric Oncology/Hematology, Otto-Heubner-Center for Pediatric and Adolescent Medicine, Charité-Universitätsmedizin Berlin, Berlin, Germany – sequence: 19 givenname: Sergio surname: Rutella fullname: Rutella, Sergio organization: Division of Translational Medicine, Sidra Medical and Research Center, Doha, Qatar – sequence: 20 givenname: Daria surname: Pagliara fullname: Pagliara, Daria organization: Department of Pediatric Hematology/Oncology, IRCCS Bambino Gesù Children’s Hospital, Rome, Italy – sequence: 21 givenname: Takashi surname: Matozaki fullname: Matozaki, Takashi organization: Department of Biochemistry and Molecular Biology, Division of Molecular and Cellular Signaling, Kobe University Graduate School of Medicine, Kobe 650-0017, Japan – sequence: 22 givenname: Eiji surname: Suzuki fullname: Suzuki, Eiji organization: Department of Breast Surgery, Kyoto University Hospital, Kyoto, Japan – sequence: 23 givenname: Catharina Willemien surname: Menke-van der Houven van Oordt fullname: Menke-van der Houven van Oordt, Catharina Willemien organization: Department of Medical Oncology, VU University Medical Center, Amsterdam, the Netherlands – sequence: 24 givenname: Robin surname: van Bruggen fullname: van Bruggen, Robin organization: Sanquin Research, and Landsteiner Laboratory, Academic Medical Center, University of Amsterdam, Amsterdam, the Netherlands – sequence: 25 givenname: Dirk surname: Roos fullname: Roos, Dirk organization: Sanquin Research, and Landsteiner Laboratory, Academic Medical Center, University of Amsterdam, Amsterdam, the Netherlands – sequence: 26 givenname: Rene A.W. surname: van Lier fullname: van Lier, Rene A.W. organization: Sanquin Research, and Landsteiner Laboratory, Academic Medical Center, University of Amsterdam, Amsterdam, the Netherlands – sequence: 27 givenname: Taco W. surname: Kuijpers fullname: Kuijpers, Taco W. organization: Sanquin Research, and Landsteiner Laboratory, Academic Medical Center, University of Amsterdam, Amsterdam, the Netherlands – sequence: 28 givenname: Paul surname: Kubes fullname: Kubes, Paul organization: Immunology Research Group, University of Calgary, Calgary, Alberta, Canada – sequence: 29 givenname: Timo K. surname: van den Berg fullname: van den Berg, Timo K. email: t.k.vandenberg@sanquin.nl organization: Sanquin Research, and 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| Keywords | trogocytosis trogoptosis antibody-dependent cellular cytotoxicity CD47-SIRPα interaction neutrophils |
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| SubjectTerms | Animals Antibodies, Monoclonal - therapeutic use Antibody-Dependent Cell Cytotoxicity antibody-dependent cellular cytotoxicity CD11b Antigen - metabolism CD18 Antigens - metabolism CD47 Antigen - metabolism CD47-SIRPα interaction Cell Line, Tumor Female Humans Male Melanoma, Experimental - metabolism Melanoma, Experimental - pathology Mice Mice, Inbred C57BL Neoplasms - drug therapy Neoplasms - immunology Neoplasms - pathology neutrophils Neutrophils - immunology Receptors, IgG - metabolism Receptors, Immunologic - genetics Receptors, Immunologic - metabolism Transplantation, Homologous trogocytosis trogoptosis |
| Title | Neutrophils Kill Antibody-Opsonized Cancer Cells by Trogoptosis |
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