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Innate Immune Training of Granulopoiesis Promotes Anti-tumor Activity

Trained innate immunity, induced via modulation of mature myeloid cells or their bone marrow progenitors, mediates sustained increased responsiveness to secondary challenges. Here, we investigated whether anti-tumor immunity can be enhanced through induction of trained immunity. Pre-treatment of mic...

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Autores principales: Kalafati, Lydia, Kourtzelis, Ioannis, Schulte-Schrepping, Jonas, Li, Xiaofei, Hatzioannou, Aikaterini, Grinenko, Tatyana, Hagag, Eman, Sinha, Anupam, Has, Canan, Dietz, Sevina, de Jesus Domingues, Antonio Miguel, Nati, Marina, Sormendi, Sundary, Neuwirth, Ales, Chatzigeorgiou, Antonios, Ziogas, Athanasios, Lesche, Mathias, Dahl, Andreas, Henry, Ian, Subramanian, Pallavi, Wielockx, Ben, Murray, Peter, Mirtschink, Peter, Chung, Kyoung-Jin, Schultze, Joachim L., Netea, Mihai G., Hajishengallis, George, Verginis, Panayotis, Mitroulis, Ioannis, Chavakis, Triantafyllos
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cell Press 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7599076/
https://www.ncbi.nlm.nih.gov/pubmed/33125892
http://dx.doi.org/10.1016/j.cell.2020.09.058
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author Kalafati, Lydia
Kourtzelis, Ioannis
Schulte-Schrepping, Jonas
Li, Xiaofei
Hatzioannou, Aikaterini
Grinenko, Tatyana
Hagag, Eman
Sinha, Anupam
Has, Canan
Dietz, Sevina
de Jesus Domingues, Antonio Miguel
Nati, Marina
Sormendi, Sundary
Neuwirth, Ales
Chatzigeorgiou, Antonios
Ziogas, Athanasios
Lesche, Mathias
Dahl, Andreas
Henry, Ian
Subramanian, Pallavi
Wielockx, Ben
Murray, Peter
Mirtschink, Peter
Chung, Kyoung-Jin
Schultze, Joachim L.
Netea, Mihai G.
Hajishengallis, George
Verginis, Panayotis
Mitroulis, Ioannis
Chavakis, Triantafyllos
author_facet Kalafati, Lydia
Kourtzelis, Ioannis
Schulte-Schrepping, Jonas
Li, Xiaofei
Hatzioannou, Aikaterini
Grinenko, Tatyana
Hagag, Eman
Sinha, Anupam
Has, Canan
Dietz, Sevina
de Jesus Domingues, Antonio Miguel
Nati, Marina
Sormendi, Sundary
Neuwirth, Ales
Chatzigeorgiou, Antonios
Ziogas, Athanasios
Lesche, Mathias
Dahl, Andreas
Henry, Ian
Subramanian, Pallavi
Wielockx, Ben
Murray, Peter
Mirtschink, Peter
Chung, Kyoung-Jin
Schultze, Joachim L.
Netea, Mihai G.
Hajishengallis, George
Verginis, Panayotis
Mitroulis, Ioannis
Chavakis, Triantafyllos
author_sort Kalafati, Lydia
collection PubMed
description Trained innate immunity, induced via modulation of mature myeloid cells or their bone marrow progenitors, mediates sustained increased responsiveness to secondary challenges. Here, we investigated whether anti-tumor immunity can be enhanced through induction of trained immunity. Pre-treatment of mice with β-glucan, a fungal-derived prototypical agonist of trained immunity, resulted in diminished tumor growth. The anti-tumor effect of β-glucan-induced trained immunity was associated with transcriptomic and epigenetic rewiring of granulopoiesis and neutrophil reprogramming toward an anti-tumor phenotype; this process required type I interferon signaling irrespective of adaptive immunity in the host. Adoptive transfer of neutrophils from β-glucan-trained mice to naive recipients suppressed tumor growth in the latter in a ROS-dependent manner. Moreover, the anti-tumor effect of β-glucan-induced trained granulopoiesis was transmissible by bone marrow transplantation to recipient naive mice. Our findings identify a novel and therapeutically relevant anti-tumor facet of trained immunity involving appropriate rewiring of granulopoiesis.
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spelling pubmed-75990762020-11-05 Innate Immune Training of Granulopoiesis Promotes Anti-tumor Activity Kalafati, Lydia Kourtzelis, Ioannis Schulte-Schrepping, Jonas Li, Xiaofei Hatzioannou, Aikaterini Grinenko, Tatyana Hagag, Eman Sinha, Anupam Has, Canan Dietz, Sevina de Jesus Domingues, Antonio Miguel Nati, Marina Sormendi, Sundary Neuwirth, Ales Chatzigeorgiou, Antonios Ziogas, Athanasios Lesche, Mathias Dahl, Andreas Henry, Ian Subramanian, Pallavi Wielockx, Ben Murray, Peter Mirtschink, Peter Chung, Kyoung-Jin Schultze, Joachim L. Netea, Mihai G. Hajishengallis, George Verginis, Panayotis Mitroulis, Ioannis Chavakis, Triantafyllos Cell Article Trained innate immunity, induced via modulation of mature myeloid cells or their bone marrow progenitors, mediates sustained increased responsiveness to secondary challenges. Here, we investigated whether anti-tumor immunity can be enhanced through induction of trained immunity. Pre-treatment of mice with β-glucan, a fungal-derived prototypical agonist of trained immunity, resulted in diminished tumor growth. The anti-tumor effect of β-glucan-induced trained immunity was associated with transcriptomic and epigenetic rewiring of granulopoiesis and neutrophil reprogramming toward an anti-tumor phenotype; this process required type I interferon signaling irrespective of adaptive immunity in the host. Adoptive transfer of neutrophils from β-glucan-trained mice to naive recipients suppressed tumor growth in the latter in a ROS-dependent manner. Moreover, the anti-tumor effect of β-glucan-induced trained granulopoiesis was transmissible by bone marrow transplantation to recipient naive mice. Our findings identify a novel and therapeutically relevant anti-tumor facet of trained immunity involving appropriate rewiring of granulopoiesis. Cell Press 2020-10-29 /pmc/articles/PMC7599076/ /pubmed/33125892 http://dx.doi.org/10.1016/j.cell.2020.09.058 Text en © 2020 The Authors http://creativecommons.org/licenses/by-nc-nd/4.0/ This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
spellingShingle Article
Kalafati, Lydia
Kourtzelis, Ioannis
Schulte-Schrepping, Jonas
Li, Xiaofei
Hatzioannou, Aikaterini
Grinenko, Tatyana
Hagag, Eman
Sinha, Anupam
Has, Canan
Dietz, Sevina
de Jesus Domingues, Antonio Miguel
Nati, Marina
Sormendi, Sundary
Neuwirth, Ales
Chatzigeorgiou, Antonios
Ziogas, Athanasios
Lesche, Mathias
Dahl, Andreas
Henry, Ian
Subramanian, Pallavi
Wielockx, Ben
Murray, Peter
Mirtschink, Peter
Chung, Kyoung-Jin
Schultze, Joachim L.
Netea, Mihai G.
Hajishengallis, George
Verginis, Panayotis
Mitroulis, Ioannis
Chavakis, Triantafyllos
Innate Immune Training of Granulopoiesis Promotes Anti-tumor Activity
title Innate Immune Training of Granulopoiesis Promotes Anti-tumor Activity
title_full Innate Immune Training of Granulopoiesis Promotes Anti-tumor Activity
title_fullStr Innate Immune Training of Granulopoiesis Promotes Anti-tumor Activity
title_full_unstemmed Innate Immune Training of Granulopoiesis Promotes Anti-tumor Activity
title_short Innate Immune Training of Granulopoiesis Promotes Anti-tumor Activity
title_sort innate immune training of granulopoiesis promotes anti-tumor activity
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7599076/
https://www.ncbi.nlm.nih.gov/pubmed/33125892
http://dx.doi.org/10.1016/j.cell.2020.09.058
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