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Novel NKG2D-directed bispecific antibodies enhance antibody-mediated killing of malignant B cells by NK cells and T cells

The activating receptor natural killer group 2, member D (NKG2D) represents an attractive target for immunotherapy as it exerts a crucial role in cancer immunosurveillance by regulating the activity of cytotoxic lymphocytes. In this study, a panel of novel NKG2D-specific single-chain fragments varia...

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Autores principales: Lutz, Sebastian, Klausz, Katja, Albici, Anca-Maria, Ebinger, Lea, Sellmer, Lea, Teipel, Hannah, Frenzel, André, Langner, Anna, Winterberg, Dorothee, Krohn, Steffen, Hust, Michael, Schirrmann, Thomas, Dübel, Stefan, Scherließ, Regina, Humpe, Andreas, Gramatzki, Martin, Kellner, Christian, Peipp, Matthias
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10641740/
https://www.ncbi.nlm.nih.gov/pubmed/37965326
http://dx.doi.org/10.3389/fimmu.2023.1227572
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author Lutz, Sebastian
Klausz, Katja
Albici, Anca-Maria
Ebinger, Lea
Sellmer, Lea
Teipel, Hannah
Frenzel, André
Langner, Anna
Winterberg, Dorothee
Krohn, Steffen
Hust, Michael
Schirrmann, Thomas
Dübel, Stefan
Scherließ, Regina
Humpe, Andreas
Gramatzki, Martin
Kellner, Christian
Peipp, Matthias
author_facet Lutz, Sebastian
Klausz, Katja
Albici, Anca-Maria
Ebinger, Lea
Sellmer, Lea
Teipel, Hannah
Frenzel, André
Langner, Anna
Winterberg, Dorothee
Krohn, Steffen
Hust, Michael
Schirrmann, Thomas
Dübel, Stefan
Scherließ, Regina
Humpe, Andreas
Gramatzki, Martin
Kellner, Christian
Peipp, Matthias
author_sort Lutz, Sebastian
collection PubMed
description The activating receptor natural killer group 2, member D (NKG2D) represents an attractive target for immunotherapy as it exerts a crucial role in cancer immunosurveillance by regulating the activity of cytotoxic lymphocytes. In this study, a panel of novel NKG2D-specific single-chain fragments variable (scFv) were isolated from naïve human antibody gene libraries and fused to the fragment antigen binding (Fab) of rituximab to obtain [CD20×NKG2D] bibodies with the aim to recruit cytotoxic lymphocytes to lymphoma cells. All bispecific antibodies bound both antigens simultaneously. Two bibody constructs, [CD20×NKG2D#3] and [CD20×NKG2D#32], efficiently activated natural killer (NK) cells in co-cultures with CD20+ lymphoma cells. Both bibodies triggered NK cell-mediated lysis of lymphoma cells and especially enhanced antibody-dependent cell-mediated cytotoxicity (ADCC) by CD38 or CD19 specific monoclonal antibodies suggesting a synergistic effect between NKG2D and FcγRIIIA signaling pathways in NK cell activation. The [CD20×NKG2D] bibodies were not effective in redirecting CD8+ T cells as single agents, but enhanced cytotoxicity when combined with a bispecific [CD19×CD3] T cell engager, indicating that NKG2D signaling also supports CD3-mediated T cell activation. In conclusion, engagement of NKG2D with bispecific antibodies is attractive to directly activate cytotoxic lymphocytes or to support their activation by monoclonal antibodies or bispecific T cell engagers. As a perspective, co-targeting of two tumor antigens may allow fine-tuning of antibody cancer therapies. Our proposed combinatorial approach is potentially applicable for many existing immunotherapies but further testing in different preclinical models is necessary to explore the full potential.
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spelling pubmed-106417402023-11-14 Novel NKG2D-directed bispecific antibodies enhance antibody-mediated killing of malignant B cells by NK cells and T cells Lutz, Sebastian Klausz, Katja Albici, Anca-Maria Ebinger, Lea Sellmer, Lea Teipel, Hannah Frenzel, André Langner, Anna Winterberg, Dorothee Krohn, Steffen Hust, Michael Schirrmann, Thomas Dübel, Stefan Scherließ, Regina Humpe, Andreas Gramatzki, Martin Kellner, Christian Peipp, Matthias Front Immunol Immunology The activating receptor natural killer group 2, member D (NKG2D) represents an attractive target for immunotherapy as it exerts a crucial role in cancer immunosurveillance by regulating the activity of cytotoxic lymphocytes. In this study, a panel of novel NKG2D-specific single-chain fragments variable (scFv) were isolated from naïve human antibody gene libraries and fused to the fragment antigen binding (Fab) of rituximab to obtain [CD20×NKG2D] bibodies with the aim to recruit cytotoxic lymphocytes to lymphoma cells. All bispecific antibodies bound both antigens simultaneously. Two bibody constructs, [CD20×NKG2D#3] and [CD20×NKG2D#32], efficiently activated natural killer (NK) cells in co-cultures with CD20+ lymphoma cells. Both bibodies triggered NK cell-mediated lysis of lymphoma cells and especially enhanced antibody-dependent cell-mediated cytotoxicity (ADCC) by CD38 or CD19 specific monoclonal antibodies suggesting a synergistic effect between NKG2D and FcγRIIIA signaling pathways in NK cell activation. The [CD20×NKG2D] bibodies were not effective in redirecting CD8+ T cells as single agents, but enhanced cytotoxicity when combined with a bispecific [CD19×CD3] T cell engager, indicating that NKG2D signaling also supports CD3-mediated T cell activation. In conclusion, engagement of NKG2D with bispecific antibodies is attractive to directly activate cytotoxic lymphocytes or to support their activation by monoclonal antibodies or bispecific T cell engagers. As a perspective, co-targeting of two tumor antigens may allow fine-tuning of antibody cancer therapies. Our proposed combinatorial approach is potentially applicable for many existing immunotherapies but further testing in different preclinical models is necessary to explore the full potential. Frontiers Media S.A. 2023-10-27 /pmc/articles/PMC10641740/ /pubmed/37965326 http://dx.doi.org/10.3389/fimmu.2023.1227572 Text en Copyright © 2023 Lutz, Klausz, Albici, Ebinger, Sellmer, Teipel, Frenzel, Langner, Winterberg, Krohn, Hust, Schirrmann, Dübel, Scherließ, Humpe, Gramatzki, Kellner and Peipp https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Immunology
Lutz, Sebastian
Klausz, Katja
Albici, Anca-Maria
Ebinger, Lea
Sellmer, Lea
Teipel, Hannah
Frenzel, André
Langner, Anna
Winterberg, Dorothee
Krohn, Steffen
Hust, Michael
Schirrmann, Thomas
Dübel, Stefan
Scherließ, Regina
Humpe, Andreas
Gramatzki, Martin
Kellner, Christian
Peipp, Matthias
Novel NKG2D-directed bispecific antibodies enhance antibody-mediated killing of malignant B cells by NK cells and T cells
title Novel NKG2D-directed bispecific antibodies enhance antibody-mediated killing of malignant B cells by NK cells and T cells
title_full Novel NKG2D-directed bispecific antibodies enhance antibody-mediated killing of malignant B cells by NK cells and T cells
title_fullStr Novel NKG2D-directed bispecific antibodies enhance antibody-mediated killing of malignant B cells by NK cells and T cells
title_full_unstemmed Novel NKG2D-directed bispecific antibodies enhance antibody-mediated killing of malignant B cells by NK cells and T cells
title_short Novel NKG2D-directed bispecific antibodies enhance antibody-mediated killing of malignant B cells by NK cells and T cells
title_sort novel nkg2d-directed bispecific antibodies enhance antibody-mediated killing of malignant b cells by nk cells and t cells
topic Immunology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10641740/
https://www.ncbi.nlm.nih.gov/pubmed/37965326
http://dx.doi.org/10.3389/fimmu.2023.1227572
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